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A detailed overview of xylanases: an emerging biomolecule for current and future prospective

A detailed overview of xylanases: an emerging biomolecule for current and future prospective Xylan is the second most abundant naturally occurring renewable polysaccharide available on earth. It is a complex heteropolysaccharide consisting of different monosaccharides such as l -arabinose, d -galactose, d -mannoses and organic acids such as acetic acid, ferulic acid, glucuronic acid interwoven together with help of glycosidic and ester bonds. The breakdown of xylan is restricted due to its heterogeneous nature and it can be overcome by xylanases which are capable of cleaving the heterogeneous β-1,4-glycoside linkage. Xylanases are abundantly present in nature (e.g., molluscs, insects and microorganisms) and several microorganisms such as bacteria, fungi, yeast, and algae are used extensively for its production. Microbial xylanases show varying substrate specificities and biochemical proper - ties which makes it suitable for various applications in industrial and biotechnological sectors. The suitability of xyla- nases for its application in food and feed, paper and pulp, textile, pharmaceuticals, and lignocellulosic biorefinery has led to an increase in demand of xylanases globally. The present review gives an insight of using microbial xylanases as an “Emerging Green Tool” along with its current status and future prospective. Keywords: Xylan, Xylanase, Glycoside hydrolase, Green tool Introduction covers 33% of total lignocellulosic biomass found on the The major constituent of the plant cell wall is “lignocellu - globe (Collins et al. 2005; Polizeli et al. 2005; Chávez et al. loses”, as the name suggests it consists of lignin (15–20%), 2006; Walia et al. 2017). It accounts for 15–30% in hard- hemicellulose (25–30%) and cellulose (40–50%) (Gray woods and 7–10% in softwood (Walia et al. 2017). There et al. 2006; Singla et al. 2012). These components together is a need for depolymerization of this complex polymer form a three-dimensional complex network with the for its efficient utilization in different industrial applica - help of covalent and non-covalent interactions (Sánchez tion. Xylanase is a group of enzymes consisting of endo- 2009). Hemicelluloses consist of xylan, a heteropolysac- 1,4-β-d-xylanases (EC 3.2.1.8), β-d-xylosidases (E.C. charide substituted with monosaccharides such as l-ara - 3.2.1.37), α-glucuronidase (EC 3.2.1.139) acetylxylan binose, d-galactose, d-mannoses and organic acids such esterase (EC 3.1.1.72), α-l-arabinofuranosidases (E.C. as acetic acid, ferulic acid, glucuronic acid interwoven 3.2.1.55), p-coumaric esterase (3.1.1.B10) and ferulic acid together with help of glycosidic and ester bonds (Collins esterase (EC 3.1.1.73) involved in the depolymerization et al. 2005; Ahmed et al. 2007; Motta et al. 2013; Sharma of xylan into simple monosaccharide and xylooligosac- 2017). Xylan is readily available in nature, followed by cel- charides (Gomez et al. 2008; Juturu and Wu 2014; Walia lulose the second most abundant polysaccharide which et al. 2017; Romero-Fernández et al. 2018). Xylanases are produced by different living organisms such as microorganisms, protozoans, and molluscs, and *Correspondence: vermaprad@yahoo.com; pradeepverma@curaj.ac.in also  found in the rumen of higher animals (Beg et  al. Nisha Bhardwaj and Bikash Kumar contributed equally to this work 2001). The xylanases are mainly produced by micro - Bioprocess and Bioenergy Laboratory, Department of Microbiology, organisms, e.g., bacteria, fungi, and actinomycetes at Central University of Rajasthan, NH-8, Bandarsindri, Kishangarh, Ajmer 305817, India © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 2 of 36 industrial scale (Motta et al. 2013). The utilization of lig - glucopyranosyl, 4-O-methyl-d-glucuronopyranosyl, nocellulosic biomass (LCB) for production of different p-coumaroyl or α-l-arabinofuranosyl side-chain groups biochemicals such as bioethanol, enzymes, and value- with varying degrees. Xylanolytic enzymes play a key added compounds has tremendously improved in recent role in the breakdown of the complex structure of xylan. years. It results in providing opportunities for scientists Hence, for complete and efficient hydrolysis of xylan to explore the hydrolytic potential of xylanase for effi - into its constituent sugars requires synergistic action of cient saccharification of LCB for ethanol and xylooligo - various enzymes with specifically targeting appropriate saccharides generation. Xylanase also finds application bonds of xylan. in several industries like pulp and paper bleaching, food, The multifunction xylanolytic system exists in bacte - feed, and pharmaceuticals. ria (Zhang et  al. 2016a, 2016b), fungi (Driss et  al. 2011; Xylanase is required in huge amount for industrial Bhardwaj et  al. 2018) and actinomycetes (Hunt et  al. level application with characteristic properties to survive 2016) where xylan backbone is randomly cleaved by the harsh industrial level processing’s (Qiu et  al. 2010). the action of endo-1,4-β-d-xylanases; xylose polymer is Therefore, there is a need to select potent microorgan - broken down to its monomeric form by action of β-d- isms for xylanase production, followed by optimization of xylosidases. Acetyl and phenolic side branches were media components for enhanced production. The under - removed by the action of α-glucuronidase and acetylxy- standing of the genetic constituents of the microbe will lan esterase. α-l-Arabinofuranosidases catalyze the help in deducing the mode of action of the enzyme. This removal of the side groups. The ester bonds present on will help in regulating the enzyme action for employment the xylan are cleaved by the action of p-coumaric ester- in desired industrial application. The microorganisms ase and ferulic acid esterase (Beg et  al. 2001; Collins also produce other protein and metabolites with desired et  al. 2005; Chakdar et  al. 2016; Walia et  al. 2017). The xylanase enzyme. Therefore, purification of the crude schematic structure of xylan showing bonds which are enzyme is a prerequisite to obtain purified enzymes. The attacked by a specific xylanolytic enzyme for complete characterization of purified xylanase will help in elucidat - hydrolysis of xylan to its constituent monomeric units is ing its stability and specificity toward different substrates. represented in Fig. 1. This will help in selecting the suitable industrial process in which it can be utilized. With the advent of advanced Classification of xylanase biotechnological techniques such as recombinant DNA Xylanase can be broadly classified into three types on technology, several attempts have been made to iden- the basis of (a) molecular mass and isoelectric point, tify, isolate and clone the gene encoding for xylanase in (b) crystal structure and (c) catalytic/kinetic property a suitable system. This approach helps in the engineer - (Wong et al. 1988; Jeffries 1996; Biely et al. 1997; Liu and ing of efficient microorganisms for enhanced xylanase Kokare 2017). On basis of molecular mass and isoelectric production with desired properties. This review gives point, the xylanase was classified into two groups, i.e., (a) a comprehensive insight into xylanase classification, its high-molecular weight with low isoelectric (acidic) point mode of action, different xylanase sources with available (HMWLI) and (b) low-molecular weight with high iso- production methods and its optimization strategies for electric (basic) point (LMWHI). However, several excep- enhanced production. The review also gives a brief idea tions to this classification have been observed where about different strategies employed for xylanase purifi - not all xylanases fall in the category of HMWLI (above cation and characterization, biotechnological approach 30  kDa) or LMWHI (below 30  kDa) (Collins et  al. 2002, for enhanced xylanase production with desired prop- 2005). Therefore, a more appropriate system includ - erties which are further used for different industrial ing primary structure (crystal), comparison of catalytic applications. domain with mechanistic features such as kinetic, cata- lytic property, substrate specificity, and product descrip - Structure of xylan and role of xylanolytic enzymes tion was introduced (Henrissat and Coutinho 2001; in its breakdown Collins et  al. 2005). The genomic, structural (3D crystal Xylan consists of d-xylose backbone linked with β-1,4- structure) and functional information of xylanase is avail- glycosidic bonds and l-arabinose traces forming into able under glycoside hydrolase (GH) families available on a complex heteropolymeric structure. Xylan is present carbohydrate-active enzyme (CAZy) database. in various biomasses that have several forms such as The CAZy is knowledge-based, highly curated database in hardwoods as O-acetyl-4-O-methylglucuronoxy- on enzymes that play a key role in breakdown, modifica - lan, in softwoods as arabino-4-O-methylglucuronox- tion, and assembly of glycosidic bonds in carbohydrates ylan and in grasses and annual plants as arabinoxylans. and glycoconjugates. It consists of genomic, sequence These residues can be substituted with acetyl, feruloyl, annotation, family classifications, structural (3D crystal) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 3 of 36 Fig. 1 Structure of xylan showing bonds which are attacked by specific xylanolytic enzyme for complete hydrolysis of xylan to its constituents (Adapted from Beg et al. 2001, Lange 2017) and functional (biochemical) information on carbohy- inversion (Subramaniyan and Prema 2002; Lombard et al. drate-active enzyme from publicly available resources 2014). such as National Center for Biotechnology Information, NCBI (Lombard et al. 2014). Retention The major GH families associated with xylanase are This process is represented by double displacement 5, 7, 8, 9, 10, 11, 12, 16, 26, 30, 43, 44, 51, and 62. The mechanism with α-glycosyl and oxo-carbonium inter- GH families 5, 7, 8, 10, 11, and 43 have a single distinct mediate formation followed by its subsequent hydrolysis. catalytic domain, whereas enzymes grouped under GH Glutamate residues play a vital role in the catalytic mech- families 16, 51, and 62 have two catalytic domains with anism. First, two carboxylic acid residues present in the bi-functional property (Collins et  al. 2005). The enzyme active site result in α-glycosyl enzyme intermediate for- grouped under GH families 9, 12, 26, 30, and 44 has mation. The intermediate formation occurs via protona - secondary xylanase activity. Based on the hydrophobic tion of the substrate by a carboxylic acid residue acting cluster analysis of the catalytic domains along with simi- as an acid catalyst and departure of the leaving group due larities studies of amino acid sequences, xylanases have to nucleophilic attack caused by another carboxylic acid. been primarily classified as GH 10 and GH 11 (Verma This collectively results in β to α inversion due to the and Satyanarayana 2012a). The catalytic properties of α-glycosyl enzyme intermediate formation. Second, the GH 10 and GH 11 have been studied extensively, whereas first carboxylate group abstracts a proton from a nucleo - the information on GH families 5, 7, 8 and 43 is very philic water molecule and attacks the anomeric carbon limited (Taibi et  al. 2012). Different structural and func - resulting in second substitution, where the anomeric tional properties of different GH families are tabulated in carbon gives rise to product with the β configuration (α Table 1. to β inversion) via a transition state of oxo-carbonium ions (Fig.  2) (Collins et  al. 2005; Lombard et  al. 2014). Mode of action of xylanases grouped under various GH Enzymes of families 5, 7, 10, and 11 mostly work on the families principle of retention. There is the difference in structure, physicochemical properties, substrate specificities and mode of action Inversion of members of GH families 5, 7, 8, 10, 11 and 43 (Col- The enzymes of families 8 and 43 act via inversion of lins et al. 2005). The hydrolysis of xylan by xylanase may the anomeric center with glutamate and aspartate as occur by two different mechanisms, i.e., retention or the major catalytic residue. This is a single displacement mechanism, in which only one carboxylate ion offers Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 4 of 36 Table 1 Classification of glycoside hydrolases (GH) family consisting of xylanase GH family Clan Activities in family Properties Mode of action References Structure Functional GH 5 GH-A endo-β-1,4-Xylanase; Consist of seven amino acid Largest GH family CNB-Glu Collins et al. (2005), Lombard et al. β-glucosidase cellulase (β/α) barrel fold Substitute on main xylan chain CPD-Glu (2014) Highly conserved Retaining GH 7 GH-B endo-β-1,4-Glucanase High-molecular weight and low pI Common characteristics with fam- CNB-Glu Collins et al. (2005), Lombard et al. β-Jelly roll ily 10 and 11 CPD-Glu (2014) small substrate-binding site (4 Retaining subsite and 1 catalytic site) GH 8 GH-M Cellulases; chitosanases; (α/α) fold Cold-adapted CNB-Asp Collins et al. (2002, 2005), Lombard lichenases; endo-1,4-β-xylanases Large substrate-binding cleft Break xylan into X3 and X4 CPD-Glu et al. (2014) Highly active on long-chain XOS Inversion of the anomeric GH 10 Family G GH-A endo-1,4-β-Xylanases; endo-1,3-β- Low-molecular mass high pI Attack on aryl β-glycosides and CNB-Glu Ahmed et al. (2009), Collins et al. xylanases (8–9.5) aglyconic bond of X2 and X3, CPD-Glu (2005), Lombard et al. (2014), (α/β) barrel fold respectively Retaining Motta et al. (2013) Small yet numerous (4–5) Highly active on short XOS substrate-binding sites GH11 GH-C xylanases “true xylanases” (active High MW and lower pI values Attack on aryl β-glycosides and CNB-Glu Ahmed et al. (2009), Collins et al. on xylose substrate) β-Jelly roll aglyconic bond of X2 and X3, CPD-Glu (2005), Lombard et al. (2014), Small size respectively Retaining Motta et al. (2013) Large substrate-binding clefts (7 Inactive on aryl cellobiosides subsites) High substrate selectivity and catalytic efficiency Wide pH and temperature stability Cold-adapted Highly active on long-chain XOS GH 43 GH-F β-Xylosidase β-Propeller (5 blade) fold Debranching and degradation of CNB-Asp Collins et al. (2005), Lombard et al. α-l -Arabinofuranosidase; xylanase Catalytic residue glutamate and hemicellulose polymer CPD-Glu (2014), Mewis et al. (2016) aspartate in the center Inverting single displace- ment mechanism X2, xylobiose; X3, xylotriose; X4, xylotetraose; XOS, xylooligosaccharides; CNB, catalytic nucleophile/base; CPD, catalytic proton donor; Asp, aspartic acid; Glu, glutamic acid Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 5 of 36 licheniformis DMS xylanase had both the properties of endoxylanase and appendage dependent xylanase activ- ity. It showed equal production of both xylobiose and xylotriose by hydrolysis of the commercial substrate and agro-waste such as corn cob (Ghosh et al. 2019). Thermothelomyces thermophila (TtXyn30A) that hydrolyzes xylan into xylose and two acidic xylooligosac- charides, namely xylotriose (M eGlcA Xyl3) and xylobi- ose, i.e., MeGlcA Xyl , was studied. TtXyn30A catalyzed the release of the disaccharide xylobiose from the non- reducing end of xylooligosaccharides, thus exhibiting an exo-acting catalytic behavior. TtXyn30A also showed the capability to cleave linear parts of xylan and uronic xylo- oligosaccharides as well as resulting in the formation of aldotriuronic and aldotetrauronic acid (Katsimpouras Fig. 2 Mode of action of xylanase: retention et al. 2019). Puchart et al. (2018) have reported the mode of action of hydrolysis of eucalyptus plant using endoxy- lanase belonging to GH10, GH11, and GH30 family. All the endoxylanse resulted in the formation of acetylated XOS. The GH10 endoxylanase results in short xylo - oligosaccharides, whereas GH30 endoxylanase results in longer xylooligosaccharides. An acetyl esterase (AcXEs) played a key role in understanding the plant decay or depolymerization mechanism and also showed efficiency in plant biomass bioconversion (Rytioja et al. 2014). A novel modular endoxylanase with transglycosyla- tion activity was reported from Cellulosimicrobium sp. HY-13 belonging to GH6 family (Ham et  al. 2012). A GH30 family xylanase XynA was reported from Erwinia chrysanthemi belonging to subfamily 8 with the special property of hydrolyzing 4-O-methyl-glucuronoxylan (Urbániková et  al. 2011). Xyn11B from thermophilic Fig. 3 Mode of action of xylanase: inversion fungus Humicola insolens Y1 encoding multi-cellular xylanase belonged to GH11 reported by Shi et al. (2015). Bacteroides intestinalis DSM17393, a xylan degrading for overall acid catalyzed group departure (Fig.  3). This human gut bacterium, reported the presence of two puta- enzyme also acts as the base for activating a nucleophilic tive GH8 xylanases which hydrolyze both xylopentose water molecule to attack the anomeric carbon (depend- and xylohexose (Hong et  al. 2014). Endoxylanase XynB ing on the distance between two molecules) for breaking from marine bacterium Glaciecola mesophila KMM241 the glycosidic bonds and causing inversion of anomeric with xylan binding ability and GH8 catalytic domain was carbon configuration (Collins et  al. 2005; Motta et  al. reported by Guo et al. (2013). 2013; Lombard et al. 2014). Several attempts have been made to understand the Mechanism for glycosidic hydrolase family 10 mode of action of xylanase obtained for different organ - (GH10) isms. An unusual mode of action of GH8 xylanase Among all the above-mentioned GH families, GH 10 (β-xylosidase, an α-arabinofuranosidase, and an acety- consists of endoxylanase, e.g., endo-1,4-β-xylanases, lesterase activity) was observed in Pseudoalteromonas endo-1,3-β-xylanases and cellobiohydrolases (Collins atlantica, which showed the presence of a long tail of et  al. 2005). Endo-1,4-β-xylanases or xylanase mainly unsubstituted xylose residue on the reducing end of oli- comes under this GH10 family. It usually consists of gosaccharides produced (Ray et  al. 2019). Thermophilic high-molecular weight xylanase with low isoelectric xylanase obtained from Bacillus licheniformis DMS has points and displays an (α/β) -barrel fold. This structure novel hydrolysis properties similar to GH30. It breaks mimics the shape of a ‘Salad Bowl’, because of an enlarged the linear β-(1-4) linkage of beech wood and birchwood loop architecture, one face of the molecule is having xylan along with glucuronoxylan and arabinoxylan. B. Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 6 of 36 ~ 45 Å large radius and the other face is having ~ 30 Å 2006). Hu et  al. (2011) proposed a model holocellulosic radius because of simple (α/β) turns (Zhang et al. 2016a, substrate, i.e., mixture of pure cellulose and 10% pre- 2016b). However, these two categories are relatively the deacetylated commercial birchwood xylan to understand same because along with sharing similar fold also shares the synergism between two family xylanase and cellulase some common residues and has similar catalytic mecha- (during the xylan extraction process). This study showed nisms. The xylanase belonging to GH 10 family has low that substrate deacetylation has increased the hydrolytic substrate specificity and, however, exhibits high catalytic performance of GH11 as the acetyl group restricted the versatility than that of GH 11 family. Xylanase belonging accessibility of xylan more for GH11 than GH10. Ther - to GH10 family exhibits greater catalytic versatility and mostability is the second factor for better performance of lower substrate specificity as compared to those belong - GH10 endoxylanase over GH11 because lignocellulosic ing to GH11 (Biely et  al. 1997; Faulds et  al. 2006; Motta biomass hydrolysis occurs better at high temperature et  al. 2013). GH10 xylanase attacks the xylose linkages (50 °C) and 2–3 days long-time duration. which are closer to the side-chain residues (Dodd and Cann 2009). This could be explained by fact that the Source for xylanase production xylose residues bind at subsites (Fig.  4) on xylanase that The xylanase is ubiquitous in nature and its presence is causes cleavage of the bond between the monomeric observed diversely in a wide range of living organisms, residues at the non-reducing (− 1) and the reducing end such as marine, terrestrial and rumen bacteria (Chakdar (+ 1) of the polysaccharide substrate (Davies et al. 1997). et  al. 2016), thermophilic and mesophilic fungi (Chadha Maslen et al. (2007) demonstrated that when arabinox- et  al. 2019; Singh et  al. 2019), protozoa (Devillard et  al. ylan was hydrolyzed by GH10 and GH11 xylanase, the 1999; Béra-Maillet et  al. 2005), crustaceans (Izumi et  al. products generated have arabinose residues substituted 1997), snails (Suzuki et  al. 1991), insects (Brennan et  al. on xylose at the + 1 subsite and + 2 subsites, respectively. 2004), algae (Jensen et al. 2018), plants and seeds (imma- Therefore, xylanases from family 11 and 10 preferentially ture cucumber seeds and germinating barley) (Bae et  al. cleave the unsubstituted regions of the arabinoxylan 2008; Sizova et  al. 2011). Bacteria and fungus are widely backbone and the unhampered substituted regions along used for industrial production of xylanase. Several micro- the xylan backbone (Biely et al. 1997; Motta et al. 2013). bial sources of xylanase are classified in Table 2. The degree of side-chain decorations of xylan influences the specificity of the enzyme toward substrates and, thus, Bacterial sources of xylanase has an important implication on the hydrolytic prod- Among bacteria, Bacillus species have been reported uct formation by xylan deconstruction (Dodd and Cann widely as the most potent xylanolytic enzyme producers 2009). Yang and Han (2018) demonstrated the positional such as Bacillus sp., B. halodurans (Gupta et  al. 2015), binding and substrate interaction of GH10 xylanase of B. pumilus (Thomas et  al. 2014), B. subtilis (Banka et  al. Thermotoga maritime using molecular docking approach. 2014), B. amyloliquefaciens, B. circulans, and B. stearo- Researchers have reported in their previous studies thermophilus (Chakdar et  al. 2016). Xylanase with high that GH10 endoxylanase had better performance than temperature stability, acid/alkali stability, and cold adapt- GH11 in synergy with cellulase enzyme for pretreated lig- ability have been isolated and purified from a wide range nocellulosic biomass hydrolysis. The reason behind this of bacteria found in extreme environment. Thermo - may be because GH11 endoxylanase has the lower acces- tolerant xylanase active at a very high temperature of sibility toward acetylated xylan backbone (Faulds et  al. 60–70 °C has been reported from Bacillus spp. (Thomas Fig. 4 Schematic representation of site for attack of GH10 xylanase on xylan Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 7 of 36 Table 2 Microbial sources of xylanase Xylanase producing microorganisms Major group Genus Species References Bacteria Arthrobacter Arthrobacter sp. Murugan et al. (2011) Geobacillus Geobacillus thermoleovorans, Geobacillus stearothermophilus Gerasimova and Kuisiene (2012), Verma and Satyanarayana (2012a, b), Bibi et al. Geobacillus thermodenitrificans (2014) Pediococcus Pediococcus acidilactici Adiguzel et al. (2019) Bacillus Bacillus firmus, Bacillus arseniciselenatis, Bacillus licheniformis, Bacillus amylolique - John et al. (2006), Bajaj and Manhas (2012), Kamble and Jadhav (2012), Amore faciens, Bacillus subtilis et al.(2015) Clostridium Clostridium thermocellum, Clostridium papyrosolvens Pohlschroder et al. (1994), Heinze et al. (2017) Dictyoglomus Dictyoglomus thermophilum Zhang et al. (2010b) Paenibacillus Paenibacillus sp., Paenibacillus xylanilyticus, Paenibacillus terrae, Paenibacillus Shi et al. (2010), Valenzuela et al. (2010), Sharma et al. (2013), Song et al. (2014) barcinonensis, Paenibacillus macquariensis Rhodothermus Rhodothermus marinus Abou Hachem et al. (2000) Staphylococcus Staphylococcus aureus, Staphylococcus sp. Gupta et al. (2000), Iloduba et al. (2016) Pseudomonas Pseudomonas sp., Pseudomonas aeruginosa, Pseudomonas fluorescens subsp. Raghothama et al. (2000), Xu et al. (2005), Iloduba et al. (2016), Lin et al. (2017), cellulose, Pseudomonas boreopolis, Pseudomonas stutzeri Purkan et al. (2017), Lee et al. (2018) Thermoactinomyces Thermoactinomyces thalophilus, Thermoactinomyces vulgaris Kohli et al. (2001), Selim (2016) Thermotoga Thermotoga maritima Velikodvorskaya et al. (1997), Shi et al. (2013), Yoon et al. (2014) Thermotoga thermarum Thermotoga neapolitana Actinomycetes Streptomyces Streptomyces sp., Streptomyces lividans Shibuya et al. (2000), Verma and Satyanarayana (2012a, b) Kitasatospora Kitasatospora sp. Rahmani et al. (2018) Nonomuraea Nonomuraea flexuosa, Nonomuraea jabiensis sp. Paloheimo et al. (2007), Camas et al. (2013) Actinomadura Actinomadura geliboluensis, Actinomadura sp. Verma and Satyanarayana (2012a, b), Adigüzel and Tunçer (2017) Cellulomonas Cellulomonas fimi, Cellulomonas flavigena, Cellulomonas uda Notenboom et al. (1998), Murugan and Jampala (2015), Lisov et al. (2017) Microbacterium Microbacterium xylanilyticum sp., Microbacterium soli sp. Kim et al. (2005), Srinivasan et al. (2010) Micrococcus Micrococcus luteus, Micrococcus sp. Gessesse and Mamo (1998), Mmango-Kaseke et al. (2016) Thermomonospora Thermomonospora fusca, Thermomonospora curvata Irwin et al. (1994), Stutzenberger (1994) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 8 of 36 Table 2 (continued) Xylanase producing microorganisms Major group Genus Species References Fungus Talaromyces Talaromyces byssochlamydoides, Talaromyces emersonii Yoshioka et al. (1981), Waters et al. (2011) Thermomyces Thermomyces lanuginosus Alam et al. (1994) Thermoascus Thermoascus aurantiacus, Thermoascus aurantiacus var. levisporus Vardakou et al. (2005), Chanwicha et al. (2015) Melanocarpus Melanocarpus albomyces Gupta et al. (2013) Chaetomium Chaetomium thermophilum, Chaetomium globosum Gandhi et al. (1994), Latif et al. (2006) Fusarium Fusarium sp., Fusarium solani, Fusarium proliferatum, Fusarium oxysporum, Saha (2002), Imad et al. (2011), Paulo et al. (2014), Adesina et al. (2017), Gascoigne Fusarium heterosporum, Fusarium roseum and Gascoigne (2019) Humicola Humicola sp. Humicola insolens, Humicola lanuginosa, Humicola grisea da Silva et al. (1994), Monti et al. (2003), Kamra and Satyanarayana (2004), Shi et al. (2015) Paecylomyces Paecylomyces variotii, Paecilomyces themophila Krishnamurthy and Vithayathil (1989), Zhang et al. (2010a) Scytalidium Scytalidium thermophilum, Scytalidium acidophilum Joshi and Khare (2012) Al Balaa et al. (2006) Thielavia Thielavia sp., Thielavia terrestaris Garcia-Huante et al. (2017), Thanh et al. (2019) Berka et al. (2011) Corynascus Corynascus sepedonium Sharma et al. (2008) Myceliophthora Myceliophthora heterothallica, Myceliophthora fergusii van den Brink et al. (2013) Sporotrichum Sporotrichum thermophile El-Naghy et al. (1991), Sadaf and Khare (2014), Topakas et al. (2003) Rhizomucor Rhizomucor pusillus Hüttner et al. (2018) Trichoderma Trichoderma inhamatum, Trichoderma piluliferum, Trichoderma viride, Tricho- Azin et al. (2007), da Silva et al. (2015), Carvalho et al. (2017), Tang et al. (2017), derma longibrachiatum, Trichoderma asperellum, Trichoderma stromaticum, Syuan et al. (2018), da Costa et al. (2019), Ezeilo et al. (2019) Trichoderma harzianum, Trichoderma reesei Aspergillus Aspergillus niger, Aspergillus flavus, Aspergillus niveus, Aspergillus ochraceus, Asper - Gawande and Kamat (1999), Betini et al. (2009), Ang et al. (2013), Dhulappa and gillus foetidus, Aspergillus fumigates, Aspergillus terreus, Aspergillus tamari Lingappa (2013), de Guimaraes et al. (2013), De Queiroz Brito Cunha et al. 2018a, b Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 9 of 36 et  al. 2014), Bacillus Halodurans TSEV1 (Kumar and understanding of the physiology and different metabolic Satyanarayana 2014), Clostridium thermocellum (Fer- processes of the microbial system has led to an improve- nandes et  al. 2015), Rhodothermus marinus (Karlsson ment in the fermentation process. However, there is still et  al. 2004), Streptomyces sp. (Sukhumsirichart et  al. an opportunity to improve the yield of enzymes. The 2014), Stenotrophomonas maltophila (Raj et  al. 2013), optimization of the xylanase production will be discussed Thermotoga thermarum (Shi et  al. 2013). Psychrophilic in a later section. xylanases are not very common but found to be isolated The xylanase production has been carried out under from several bacteria such as Clostridium sp. PXLY1 submerged fermentation (SmF) and solid-state fer- (Akila and Chandra 2003), Flavobacterium sp. MSY-2 mentation (SSF) (Motta et  al. 2013). The choice of the and Flavobacterium frigidarium (Humphry et  al. 2001; fermentation process usually depends on the type of Dornez et  al. 2011) Pseudoalteromonas haloplanktis microorganisms used (Table  3). Bacteria require a high TAH3A (Van Petegem et al. 2002). amount of water during growth; therefore, SmF is pre- Several alkali stable xylanases have been isolated from ferred whereas fungi due to its mycelia nature require firmicutes such as B. pumilus (Thomas et  al. 2014), B. less moisture and can be grown under SSF (Walia et  al. halodurans TSEV1 (Kumar and Satyanarayana 2014) and 2017). Several reports suggest that submerged fermen- Geobacillus thermoleovorans (Verma and Satyanarayana tation using bacteria and fungi is the most preferred 2012b) and actinomycetes such as Actinomadura sp. method for xylanase production. Statistically speaking Cpt20 (Taibi et  al. 2012) and Streptomyces althioticus approximately 90% of total xylanase is produced globally LMZM (Luo et al. 2016). through SmF. During SmF, the synergistic effect of differ - ent xylan degrading enzymes can be observed and even result in better biomass utilization for enhanced xyla- Fungal sources of xylanases nase production (Polizeli et  al. 2005; Bajpai 2014). Xyla- The mesophilic fungi of genera Aspergillus and Tricho- nase production utilizes soybean residues and rice straw derma are well known to be potent xylanase producer as a substrate under SmF by Aspergillus oryzae LC1 and and most widely used for commercial production. iel Th a - Aspergillus foetidus (Bhardwaj et  al. 2017; De Queiroz via terrestris, (Garcia-Huante et  al. 2017), Talaromyces Brito Cunha et al. 2018a, b). Similarly, Irfan et al. (2016) thermophilus (Maalej et  al. 2009), Paecilomyces thermo- suggested the production of xylanase under SmF by B. phile (Fan et  al. 2012), Achaetomium sp. X2-8 (Chadha subtilis BS04 and B. megaterium BM07. Different advan - et  al. 2019), Rhizomucor pusillus (Hüttner et  al. 2018), tages of the SmF are homogenous condition throughout Rasamsonia emersonii, (Martínez et al. 2016) T. Leycetta- medium; method is well characterized and can be easily nus (Wang et al. 2017), Melanocarpus albomyces (Gupta scaled up (Guleria et al. 2013). There are some disadvan - et  al. 2013) and Aspergillus oryzae LC1 (Bhardwaj et  al. tages to SmF as well which limit its industrial application, 2019) were found to be producer of hyper-thermophilic i.e., high maintenance cost, energy intensive and complex active xylanase. Several alkali stable xylanases were downstream (Virupakshi et al. 2005; Walia et al. 2017). obtained from different fungal strains such as Paeniba - Recent trends suggest that xylanase production by SSF cillus barcinonensis (Valenzuela et  al. 2010), Aspergillus is also gaining popularity (Walia et  al. 2014). Bacillus fumigatus MA28 (Bajaj and Abbass 2011), Cladosporium sp. was used for the production of thermo-alkalophillic oxysporum (Guan et al. 2016) and Aspergillus oryzae LC1 extracellular xylanase under SSF using wheat bran as (Bhardwaj et al. 2019). substrate (Kamble and Jadhav  2012). Similarly, SSF of Trichoderma koeningi using corn cob supplemented with pineapple peel powder showed enhanced production Strategies employed for xylanase production of xylanase (Bandikari et  al. 2014).  It has several advan- from different microbial sources tages such as low cultivation, operation and capital cost, The production of xylanase from microorganisms is a lower rate of contamination, easy enzyme recovery, and affected by the fermentation process employed, choice of high productivity per reactor volume. The disadvantages substrate and different media components. These com - associated with SSF are not suitable for all microorgan- ponents are often regulated by different process opti - isms (preferred for the fungal system) and require proper mization for enhanced production of the enzyme for its aeration and humidity control and up-scaling is a tedious application at large scale. process (Mienda et al. 2011). Different fermentation process employed for xylanase Selection of suitable substrate for xylanase production production: submerged and solid‑state fermentation Quantity and quality of the fermentation product vary Xylanases are produced by a different fermentation with different substrates. There are various commercially process using various microorganisms. The better Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 10 of 36 Table 3 Production system, characteristic properties and application of xylanase from different microorganisms Microbes Substrate Fermentation MW (kDa) Optimum Stability Metal activator Application References Temperature (°C) pH Temperature (°C) pH Bacteria Bacillus altitudedi- Sorghum straw SmF 98 50 8 35–70 3–10 Ca, Mn, K, Na, Fe Deinking of waste Adhyaru et al. (2017) nus hand-written paper pulp Paenibacillus baren- Birch wood xylan, SmF 116 60 6.5 20–65 4–11 Mg, Ca, Ba, Co XOS production Liu et al. (2018) goltzii beechwood xylan, oat-spelt xylan Burkholderia sp. Wheat Bran SmF – 50 8.6 30–50 6–9 Co, Na, Ba, Mg, K Hydrolysis of ligno- Mohana et al. (2008) DMAX cellulosic biomass Bacillus licheni- Wheat Bran SmF 46 60 9 30–100 4–11 Fe, Mn Kraft pulp bio- Raj et al. (2018) formis Mg, Zn bleaching Ca, Ni Anoxybacillus Beech wood xylan SmF 37 65 9 30–65 6–9 – Thermo-alkaline Yadav et al. (2018) kamchatkensis stable xylanase NASTPD13 suitable for indus- trial application Pediococcus acidi- Oatmeal SmF 48.15 40 7 20–50 2–9 K, Ba, Cd, Co, Sr, Mg, Clarification of fruit Adiguzel et al. (2019) lactici GC25 Ca, Al, Zn, Ni juice Pseudomonas Wheat Bran SmF 20 65 6 55–75 5–9 – Thermo-alkali stable Lin et al. (2017) boreopolis LUQ1 xylanase for indus- trial application Geobacillus sp. Corncob, beech- SmF 45 75 7 50–85 5–9 Cu, Zn, K, Fe, Ca, Zn, Ethanol Generation Bibra et al. (2018) Strain DUSELR13 wood Mg, Na Actinomycetes Streptomyces oliva- Birch wood Xylan SmF 23 40 7 20–70 5–11 Na, Cu, Co, Fe, Zn, Pretreated biomass Sanjivkumar et al. ceus (MSU3) Mg, Mn hydrolysis for (2017) bioethanol pro- duction Streptomyces Beech wood xylan SmF 46.2 65 6.5 50–70 4–11.5 Ca, Co, Mn XOS production Boonchuay et al. thermovulgaris (2016) TISTR1948 Kitasatospora sp Sugarcane bagasse SmF 49.3 50 5 30–80 4–7 Zn, EDTA XOS production Rahmani et al. (2019) Actinomadura sp. 20.11 80 10 60–90 5–10 Mn, Ca, Cu Paper and Pulp Taibi et al. (2012) strain Cpt20 Industry Fungus Trichoderma Rice straw SSF – 60 5 30–60 3–10 – Textile processing El et al. (2018) longibrachiatum efficient desizing KT693225 and bioscouring, Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 11 of 36 Table 3 (continued) Microbes Substrate Fermentation MW (kDa) Optimum Stability Metal activator Application References Temperature (°C) pH Temperature (°C) pH Trichoderma viride Rice bran, sugarcane SSF 14 50 7 25–50 3–9 Zn, Fe, Mg, Mn, Ca Bio-bleaching of Nathan et al. (2017) VKF3 bagasse, coconut newspaper oil cake, ground- nut oil cake, neem oil cake Trichoderma pilu- Wheat bran SSF – 50 4.5 30–60 3–10 – Additives for bovine da Costa et al. (2019) liferum feeding Humicola insolens wheat bran SmF 44 70–80 6–7 40–80 5–10 Brewing Industries Du et al. (2013) Y1 and XOS genera- tion Pichia stipitis corn cob wheat bran SSF 31.6 50 6 40–60 3.0–11.0 Cu, K XOS generation Ding et al. (2018) Fusarium sp Wood shaving SSF – – – 25–55 4–9 – Paper and pulp Adesina et al. (2017) bleaching Thermomyces wheat bran SmF – 47.9 7.3 30–65 3.0–10.0 Mg, Na, K Fermentable sugar Kumar and Shukla lanuginosus production, pulp (2018) bleaching Thermoascus Wheat Bran SmF 31 75 5 30–80 2–10 Mn, Ag – Ping et al. (2018) aurantiacus Schizophyllum com- Rice straw SSF – 55 5 30–65 4–7 Na, K, Ca Kraft pre-bleaching Gautam et al. (2018) mune ARC-11 Aspergillus oryzae Rice straw SmF 35 25 5 25–60 3–10 Fe, Ag, Mg, Mn, Co Hydrolysis of Agro- Bhardwaj et al. (2017, LC1 residues and XOS 2019) Production SmF, submerged fermentation; SSF, solid-state fermentation; XOS, xylooligosaccahrides Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 12 of 36 available substrates, i.e., xylan, carboxymethyl cellulose the type and level of nitrogen source in the media is an (CMC), pectin, and starch for, i.e., xylanase, cellulase, important parameter (Seyis and Aksoz 2005; Naveen pectinase, and amylase, respectively (Barman et al. 2015; et  al. 2014; Irfan et  al. 2016). Trace elements, amino Bhardwaj et al. 2017; Kumar et al. 2018a). Due to the high acids, and vitamins are also important parameters for the cost of commercial substrates and considering the eco- growth of different microorganisms (Simair et  al. 2010; nomic feasibility of the process, scientists are working Bibra et al. 2018). Therefore, regulating their levels in the from past several years to find alternative substrates for media is important for regulating the production of xyla- the production of these enzymes. nase. Also, the addition of biosurfactant such as Tween Agrowastes and other organic wastes (domestic and 80 affected the level of xylanase production (Liu et  al. industrial) are used as a carbon source for the production 2006; Kumar et al. 2013). of xylanase with the focus on sustainability and best uti- lization of these wastes (Table 3). Some of the most com- Strategies employed for the selection monly used agro-residues for xylanase production are of the method of xylanase production and its wheat bran, wheat husk (Kumar et al. 2018a, b, c, d), rice optimization straw (Bhardwaj et al. 2017), rice husk, sugarcane bagasse Intially a  common minimal media providing essential (Suleman and Aujla 2016), coconut coir, coconut oil cake nutrients to the growth of microorganisms are used. (Rosmine et  al. 2019), groundnut shell (Namasivayam This  will allow to  check the strains are capable of pro - et  al. 2015), wood pulp (Kalpana and Rajeswari 2015), ducing required enzymes/metabolite of desired interest. sawdust, chilli post-harvest (Sindhu et  al. 2017), corn- Then, the process is further optimized for higher produc - cobs, molasses, sugar beet pulp fruit, and vegetable waste tion of enzymes from the strain (Walia et  al. 2017). For (Bandikari et  al. 2014). Recent studies also showed that the production of desired product, different strategies are wastewater from pulp industry was reused as media for used for improving yield such as optimization of media xylanase production (de Queiroz-Fernandes et al. 2017). components, regulating physical growth parameters, and improving the strain by use of the different biotechno - Role of important media components used for xylanase logical tool (Sharma 2017). The schematic representation production of the methodology adapted for production, purification Naturally, xylanolytic enzymes are induced by the differ - and characterization of xylanase are shown in Fig.  5.  In ent intermediate products generated by their own action. this section, the focus will be on the optimization of Xylan is found to be best xylanase inducer (Taibi et  al. media and growth parameters and biotechnological 2012; Guleria et  al. 2013; Walia et  al. 2013, 2014). How- tool approach will be discussed in a later section. Dur- ever, xylan being a high-molecular weight polymer can- ing SmF for enzyme production, different components not stimulate xylanase as it cannot enter the microbial which need to be optimized are selection of substrate and cells. Therefore, a small amount of constitutive enzyme microorganisms, regulation of nutrients concentration produced in the media results in the generation of low- in media, i.e., carbon, nitrogen, trace elements, vitamins molecular weight fragments, i.e., xylobiose, xylotriose, and amino acids, and physical parameters, i.e., tempera- xylotetraose, xylose from the breakdown of xylan and ture, pH, agitation, aeration, inoculum sizes, and incuba- further induces the xylanolytic enzymes for enhanced tion period (Motta et al. 2013; Walia et al. 2015a, 2017). enzyme production (Walia et  al. 2017). Cellulose, syn- During optimization of the SSF, there is requirement thetic alkyl, aryl β-d xylosides, and methyl β-d-xyloside of regulating particle size, pretreatment, humidity, water also act as an inducer for xylanolytic enzyme production content and water activity (a ) of substrate, type and size (Thomas et  al. 2013). Busk and Lange (2013) observed of the inoculums, removal of extra heat generated during that poor quality paper can efficiently induce the xyla - microbial metabolism and most importantly maintaining nase production in Thermoascus aurantiacus even in the the uniform environment (temperature) and evolution of absence of xylan and xylooligosaccharides. CO and consumption of O , i.e., gaseous system (Muru- 2 2 Nitrogen is an important structural element required gan et al. 2011; Behera and Ray 2016; Behnam et al. 2016; for the metabolic processes in the microbial system. Leite et al. 2016; Walia et al. 2017). Therefore, the choice of nitrogen source is important for the growth of microorganisms that subsequently affect Approach for enhanced xylanase production: one factor the overall enzyme yield. Peptone, tryptone, soymeal, at a time (OFAT) yeast extract, etc. have found to be suitable nitrogen To proceed for the optimization of the xylanase produc- source. The requirement of these nitrogen sources var - tion, one factor at a time (OFAT) approach is used for ies for different microorganisms; therefore, optimizing the selection of important factors affecting the xylanase Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 13 of 36 Fig. 5 Schematic representation of the methodology for production, purification and characterization of xylanase yield. In the OFAT approach, one factor is kept variable parameters (substrate concentration) were optimized keeping other factors at constant (Bhardwaj et  al. 2018). using OFAT approach for enhanced production of xyla- The factor may be important physical or nutritional nase by T. viride-IR05 under SSF (Irfan et al. 2014). parameters regulating the growth of microorganisms and its enzyme yield. Ramanjaneyulu et  al. (2017) have Statistical approach for enhanced xylanase production evaluated several operating parameters for nutritional The OFAT approach is tedious and requires a large set of (different substrates and their concentrations, additional experiments for optimization. The recent trend suggested carbon and nitrogen sources) and physical factors (incu- the application of the statistical approach to design bation temperature, pH, agitation) along with inoculum experiments considering different factors as variable size of Fusarium  sp. BVKT R2 in a shake flask culture and performing the interaction studies among several (SmF) by OFAT approach. The high xylanase yield of physical and nutritional parameters. The statistical-based 4200 U/mL was obtained with birch wood xylan in min- approach has shown satisfactory results for optimization eral salt medium with 1.5% sorbitol (additional carbon of xylanase production using fungal and bacterial strains source), 1.5% yeast extract (nitrogen source) at tempera- with the minimum number of experimental sets (Gule- ture of 30 °C, pH of 5.0, agitation of 200 rpm and inocu- ria et  al. 2015, 2016a; Walia et  al. 2015b; Bhardwaj et  al. lum of agar plugs (6) for only 5  days incubation. Under 2017). unoptimized condition, xylanase yield was only 1290 U/ Response surface methodology (RSM) was employed mL after 7 days of incubation, thus improving by 3.2-fold. to optimize the fermentation medium constituents and Bhardwaj et  al. (2018) also optimized xylanase produc- the physical factors affecting xylanase production using tion using Aspergillus oryzae LC1 using OFAT approach. Bacillus tequilensis strain ARMATI under SmF (Khusro The physical parameters (liquid to solid ratio, pH, inocu - et  al. 2016). The experimental design consists of cen - lums size, incubation time and temperature) and nutrient tral composite design (CCD) with four (4) independent Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 14 of 36 variable (carbon and nitrogen source, temperature and biotechnological approaches are used for improving time) resulting in 30 experimental runs. The central com - the yield and imparting characteristic properties to posite design gave an optimum parameter for studied the desired enzyme. These approaches involve genetic variable (1.5% w/v birchwood xylan, 1% w/v yeast extract, manipulation involving mutation and recombinant DNA temperature 40 °C, time 24 h) showing 3.7-fold enhanced technology. xylanase production as compared to OFAT. High coef- ficient of determination (R ) of 0.9978 with p < 0.05 as Mutagenesis of microorganisms for enhanced xylanase obtained by analysis of variance (ANOVA) analysis sug- production gested the accuracy of the overall process at a significant Several researchers suggested that the application of level. The R value of 0.9978 represents that sample varia- physical mutagens such as UV radiation (Rahim et  al. tion of 99.78% and only 0.21% of the total variation in the 2009; Abdel-Aziz et  al. 2011) and chemical mutagens response cannot be explained by the model. The xylanase such as N-methyl N-nitro N-nitroso guanidine (MNNG) obtained has shown high thermal (60  °C) and alkali sta- (Haq et  al. 2004, 2008) resulted in enhanced xylanase bility (pH 9). Bhardwaj et al. (2017) optimized nutritional production. Burlacu et  al. (2017) demonstrated the components (rice straw, MgSO , and CaCl concentra- 4 2 improvement of xylanase production in fungal strains, tion) and physical parameters (temperature and pH) for i.e., Aspergillus brasiliensis and Penicillium digitatum by enhanced xylanase production with an Aspergillus oryzae physical mutagenesis (5–50  min, exposure to UV light) LC1 under submerged fermentation using CCD-RSM. and chemical mutagenesis (150  µg/mL of N-methyl-N′- The statistical design suggested optimum condition of nitro-N-nitrosoguanidine or ethyl methane sulfonate). 1% rice straw (w/v), 1.0  g/L C aCl , and 0.3  g/L M gSO , 2 4 The exposure to physical and chemical mutagens has with pH 5 and 25  °C. It resulted in maximum xylanase resulted in significant changes in the mutant strain as activity of 935 ± 2.3 IU/mL which is 3.8-fold higher than compared to the wild type. Han et  al. (2017) demon- the un-optimized Mendel’s Stenberg Basal Salt medium strated the site-directed mutagenesis of XynCDBFV (245 ± 1.9  IU/mL). The enzyme showed thermal (25– gene of ruminal fungus  Neocallimastix patriciarum for 60 °C) and pH (3–10) stability. The xylanase also showed improving the thermostability of XynCDBFV, a glyco- potential for efficient enzymatic hydrolysis of different side hydrolase (GH) family 11 xylanase. Similar work lignocellulosic agro-residues. has also been carried out in different bacterial strains, a Similarly, Tai et  al. (2019) reported the optimization rifampin-resistant mutant of Cellulomonas biazotea, des- of five physical and two nutritional parameters using the ignated 7Rf, resulting in elevated levels of xylanases pro- RSM approach for enhanced xylanase production. Indig- duction as compared to the parental strain. After enous fungus Aspergillus niger DWA8 was grown under mutation, maximum xylanase and β-xylosidase pro- SSF on an oil palm frond. One physical (moisture content duction of 493  IU/L/h and 30.7  IU/L/h of β-xylosidase 75%) and one nutritional parameters (substrate concen- were obtained  respectively. This increase in xylanase tration 2.5 g) have significant effect on xylanase produc - and  β-xylosidase yield  were 1.21- and 2.29-fold higher tion. Under optimum condition,  an increase in xylanase respectively  as compared to the parental strain (Rajoka yield by  78.5% was observed as compared to an  un- et  al. 1997). Bacillus mojavensis PTCC 1723 when sub- optimized condition. The xylanase was efficiently used jected to UV light exposure (280 nm, 30 s) resulted in the for saccharification of biomass. The statistical optimiza - xylanase yield 330.6  IU/mL which is 3.45 times higher tion method for enhanced xylanase production has been as compared to 95.7  IU/mL for wild strain (Ghazi et  al. applied and widely accepted for SSF and SmF that helped 2014). Lu et al. (2016) demonstrated mutation of XynHB, in overcoming several limitations of classical empirical alkaline stable xylanase from  Bacillus pumilus  HBP8 at (OFAT) methods. N188A. The mutant XynHBN188A is expressed in E. coli and Pichia pastoris with improved xylanase yield by 1.5- Biotechnological approach for enhanced xylanase and 7.5-fold, respectively. The codon-based optimization production and high-density fermentation using Pichia pastoris sys- There is a need of high yield of the enzyme with spe - tem were utilized for improving the xylanase yield. cific properties such as high stability over a wide range of temperature and pH, high substrate specificity and Gene cloning and expression of xylanase genes using strong resistance to metal cations and chemicals for the recombinant DNA industrial application (Garg et  al. 2010;  Qiu et  al. 2010). The recombinant xylanases are designed to have equiv - The native enzyme is usually produced in low quantity alent or better properties than the wild-type enzymes and also lacks all the characteristics to meet the indus- with high yield in the expression system which can trial needs (Ahmed et  al. 2009). Therefore, different be employed in the fermentation industry. The highly Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 15 of 36 thermo-alkalophilic xylanase producing strains can be 6.5 and 85  °C, respectively. The xylanase was stable up directly employed during simultaneous saccharification to 95  °C and retained its activity in surfactants such as and fermentation for ethanol generation using lignocel- EDTA, DTT, Tween-20 and Triton X-100. lulosic biomass. The inherited stability will enable the xylanase to work efficiently even at high temperature and Expression in yeast varying pH range of the fermentation system. The heterologous protein expression in yeast system is Several reports suggests that desired xylanase gene was highly attractive due to its ability to perform eukaryotic cloned into the suitable vector followed by its expression post-translational modifications and can grow to very in the suitable microbial systems such as bacteria, yeasts, higher cell densities with the ability to secrete enzyme and fungus (Belancic et  al. 1995; Goswami et  al. 2014; into the fermentation system. Most of the yeasts are con- Jhamb and Sahoo 2012; Juturu and Wu 2012; Motta et al. sidered as GRAS organisms and do not produce toxins 2013; Nevalainen and Peterson 2014; Verma et al. 2013). (Juturu and Wu 2012). Saccharomyces cerevisiae already established as an industrial microorganism, thus, can be conveniently used for xylanase production (Ahmed et al. Expression in bacteria 2009). Goswami et  al. (2014) demonstrated the expression of a The application of Pichia pastoris as expression sys - xylanase gene from Bacillus brevis in E. coli BL21. The tem has gained impetuous because it can promote the recombinant strain predominantly secreted xylanase in expression of the protein on their own using alcohol the culture medium with 30 IU/mL xylanase activity. The oxidase as promoter using methanol utilization pathway culture filtrate is free from cellulase activity and found (Ahmed et  al. 2009; Juturu and Wu 2012; Motta et  al. to be active in a wide range of pH and temperature. A 2013). Pichia pastoris as expression system is preferred as thermo-alkali stable xylanase encoding gene (Mxyl) was it can grow to very high cell densities, inherit strong and retrieved from compost-soil metagenome library con- tightly regulated promoters, and produce high titer of struct and cloned into pET28a vector expressed in E. coli recombinant protein (g/L) both intracellularly and in the BL21(DE3). The recombinant xylanase has shown half- secretory manner (Ahmad et al. 2014). Basit et al. (2018) life of 2 h and 15 min at 80 °C and 90 °C, respectively. The demonstrated the cloning of two GH11 xylanase genes, recombinant xylanase has pH and temperature optima of MYCTH_56237  and  MYCTH_49824, from thermophilic 9.0 and 90 °C, respectively (Verma et al. 2013). fungus  Myceliophthora thermophila  and its expres- Escherichia coli is preferred and most widely used sion in  Pichia pastoris. The specific activities of purified expression host due to its inexpensive growth conditions, recombinant xylanase were observed at 1533.7 U/mg and easy manipulation, simple transformation techniques 1412.5 U/mg for MYCTH_56237  and  MYCTH_49824, requirement, high level of product accumulation in the respectively.  The recombinant xylanase showed stability cell cytoplasm (Jhamb and Sahoo 2012). However, effi - under harsh condition (high pH and temperature) and cient and functional expression of many xylanase genes high efficiency for biomass saccharification. However, is not possible with E. coli which may be due to repetitive the application of Pichia pastoris at large scale is limited appearance of rare codons and the requirement for spe- due to health and fire hazards of methanol (Ahmed et al. cific translational modifications (disulfide-bond forma - 2009). In the case of P. pastoris as expression system, tion and glycosylation) (Belancic et  al. 1995; Jhamb and lower protein yield was obtained while expressing mem- Sahoo 2012; Juturu and Wu 2012; Motta et al. 2013). One brane-attached protein or proteolytic degradation prone of the other important concerns associated with E. coli is protein and complex protein such as hetero-oligomers the presence of endotoxins (lipopolysaccharide) which (Ahmad et al. 2014). makes the protein purification process very tedious. Lactobacillus and Bacillus species are used for heterolo- Expression in filamentous fungi gous expression of xylanase than in E. coli. It is capable Filamentous fungi can be efficiently used for heterolo - of performing N-glycosylation, generally regarded as gous and homologous gene expression resulting in high safe (GRAS) due to the absence of endotoxins and their yield of recombinant gene products (Su et al. 2012; Motta secretory production is beneficial in industries (Bron et  al. 2013; Nevalainen and Peterson 2014; Nevalainen et  al. 1998; Subramaniyan and Prema 2002; Upreti et  al. et  al. 2018). Similar to yeast, it can regulate expression 2003; Juturu and Wu 2012). Zhang et al. (2010a, b) dem- yields with their own promoters and can provide eukary- onstrated the expression and characterization of the otic style post-translational modification of proteins such xylanase gene (xynB) from Dictyoglomus thermophilum as N-glycosylation, proteolytic processing, or formation Rt46B.1 in Bacillus subtilis system. The pH and tempera - of multiple disulfide bonds (Ahmed et al. 2009; Fleissner ture optima for the purified recombinant enzyme were and Dersch 2010; Landowski et al. 2015). Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 16 of 36 Ammonium sulfate precipitation followed by dialysis The application of fungi as an expression system also The crude xylanase preparation is subjected to different has advantages associated with cost-effectiveness of the ranges of ammonium sulfate concentration (30–90%) for overall process due to low-cost substrate and down- selection of suitable salt concentration for precipitation stream processing. Further, fungi have already been of the enzyme. The precipitated enzyme is then subjected subjected to many strain improvement procedures for to dialysis for removal of the salt. The crude xylanase enhanced production of xylanase. Therefore, the native obtained from Streptomyces P12-137 was subjected to xylanase expressing machinery can be efficiently used ammonium sulfate precipitation (40–90%) followed by for functional expression of a foreign xylanase gene dialysis. The purification fold of 4.18 was observed with from other sources. Xyn2 xylanase gene was expressed two different endoxylanase observed as F5 (65%) and F6 in T. reesei by homologous expression resulting in the (80%) with the specific activity of 45.4 U/mg and 36.5 U/ 1.61 g/L of xylanase 2 on glucose-containing medium (Li mg, respectively. This was also confirmed by HPLC anal - et  al. 2012). Godlewski et  al. (2009) demonstrated xyla- ysis. The purified enzyme was further characterized by nase B(XynB) gene expression in  T. reesei. Similarly, the incubating at different temperature and pH followed by expression of xylanase 2 (XYN2) and xylanase gene from analyzing the enzyme for xylanase activity. The optimum the thermophilic fungus Humicola grisea var. thermoidea pH and temperature of pH 7.0, 60  °C and 6.5, 60  °C, for and P. griseofulvum was expressed in Trichoderma reesei F5 and F6 xylanase, respectively, were obtained (Coman and Aspergillus oryzae, respectively (De Faria et al. 2002; et al. 2013). Motta et  al. 2013). Nevalainen and Peterson (2014) pre- Bhardwaj et  al. (2017) performed partial purification sented a comprehensive review on application of fila - of the crude xylanase obtained from Aspergillus oryzae mentous fungus as expression system and suggested that LC1 using ammonium sulfate (60%) precipitation fol- research is now focused on understanding the cellular lowed by dialysis against 50 mM acetate buffer (pH 5.0). mechanisms for better internal protein quality control The partially purified enzyme was further characterized and secretion stress. The better utilization of “omics” which showed stability over a wide pH range of 3 to 10 tools can help in improving the regulation of xylanase and thermal stability over the temperature range of 25 production using filamentous fungus as an expression to 60  °C. Similarly, Kumar et  al. (2018d) have demon- system. strated the purification and characterization of xylanase obtained from sea sediment bacteria using a combina- Strategies for enhanced purification tion of ammonium sulfate precipitation and dialysis. The and characterization of xylanase for industrial improvement in specific activity and characteristic prop - application erties of xylanase was observed. The major limitations of The microbial system produces a wide range of biochem - the precipitation are needed to remove salt from protein ical’s during different growth and development of the sample so further processing in the form of dialysis or microorganisms. These biochemical’s are enzymes, sec - chromatography is required. Further, for dialysis, there ondary metabolites, etc. which are of great importance is a need to have a better understanding of the protein to human applications. Similarly, enzymes are produced solubility. It is also stated that ammonium precipitation by microorganisms along with other enzymes or metabo- concentrates the protein rather than purifying it. Thus, lites. Therefore, purification is prerequisites for obtain - contaminant present in the crude sample may also be ing pure enzyme with minimum or no impurities (Zhang present along with the protein sample even after pre- et  al. 2012). The characterization of the purified enzyme cipitation and dialysis (Biosciences 2019). The xylanase such as evaluation of  temperature and pH optimum, is also concentrated or precipitated using trichloroacetic thermal and acid/alkali stability, role of  metal ions and acid (TCA) and acetone. However, the TCA may dena- inhibitors in regulation of enzyme activity, and substrates ture the protein; therefore, it is not advisable to use TCA specificity was performed  for selecting the suitable when the protein is required in the folded state (for activ- industrial process (Bhardwaj et al. 2019). There are differ - ity assay) and the toxicity of TCA also limits its applica- ent enzyme purification strategies for the xylanase such tions (Koontz 2014). as ammonium sulfate precipitation (salting in) followed by dialysis (salting out), gel permeation chromatography, Chromatography techniques for enhanced xylanase yield ion exchange chromatography, recently developed tech- employed for purification niques aqueous phase chromatography and ultrafiltration Usually, it has been observed that xylanase purifica - (Walia et  al. 2014; Guleria et  al. 2016b; Bhardwaj et  al. tion was performed by the multi-step process where 2019). Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 17 of 36 the concentration of protein using ammonium acetate/ i.e., aqueous two-phase system (Naganagouda and Muli- TCA/acetone precipitation or ultracentrifugation was mani 2008; Yasinok et al. 2010; Glyk et al. 2015). followed by a single step or series of chromatography Garai and Kumar (2013) purified alkaline xylanase from techniques. Yadav et  al. (2018) demonstrated the puri- Aspergillus candidus using aqueous two-phase system fication and characterization of extracellular xylanase (ATPS) composed of PEG 4000/NaH PO system. The 2 4 obtained from  A. kamchatkensis  NASTPD13 cultures. critical factors of ATPS such as PEG molecular weight, The crude xylanase was subjected to ammonium sulfate PEG and phosphate salt concentration using Box– (80%) precipitation followed by dialysis. The dialyzed Behnken design approach were used for the optimization sample was further subjected to Sephadex G100 column of enhanced xylanase purification. The optimum condi - chromatography. The fractions collected showing maxi - tion was PEG 4000 at 8.66% w/w with a high salt con- mum xylanase activity were concentrated and analyzed centration of 22.4 w/w that resulted in 8.41% purification by SDS-PAGE (MW obtained was 37  kDa). The two- fold. The enzyme was stable at alkaline pH and activity is 2+ step purification has led to increased xylanase activity by enhanced with Mn ions. Ng et al. (2018) demonstrated 11-fold with a 33 U/mg specific activity. The characteri - the recovery of xylanase from Bacillus subtilis fermenta- zation of purified protein showed pH and temperature tion broth with an alcohol/salt ATPS. The ATPS system optimum of 9.0 and 65 °C, respectively, and also retained consists of 26% (w/w) 1-propanol and 18% (w/w) ammo- more than 50% of its activity over a wide range of 6–9 nium sulfate resulting in 5.74 ± 0.33 purification fold and pH and 30–65  °C temperature. An insight into several yield of 71.88% ± 0.15. purification strategies employed for xylanase from differ - Gómez-garcía et  al. (2018) demonstrated purifica - ent microorganisms along with the process efficiency in tion of xylanase by Trichoderma harzianum using ATPS terms of recovery potential and kinetics property is tabu- with PEG/salt system. The PEG molecular weight, PEG, lated in Table 4. phosphate salt concentration, and salt conditions were Purification of endoxylanase obtained from Bacillus optimized. The best   enzyme recovery and  purifica - pumilus B20 was performed in three steps (Geetha and tion fold  of 62.5% and 10% respectively  was obtained Gunasekaran 2017). The first step was ammonium sulfate using 20.2% PEG 8000, 14.8% K HPO , and tie to a length 2 4 precipitation (60–80%) followed by FPLC using DEAE of 45% w/w. Bhardwaj et al. (2019) subjected crude xyla- Sepharose column as the second step and further sub- nase from Aspergillus oryzae LC1 to four different single- jecting the eluted sample onto a Sephacryl S-200 column step purification by ammonium sulfate precipitation, ion as the third purification step. At each step, the specific exchange, gel filtration chromatography and ATPS PEG/ activity was improved as compared to the crude enzyme Salt system. The xylanase purification using single-step by 5 to 14.8-fold with maximum 755.8 U/mg specific ATPS system resulted in highest purification yield (PY) of activity at the end of all the three purification steps. After 86.8% and 13-fold purification fold (PF) which was much the purification, the fractions showing maximum xyla - higher than other purification strategy, i.e., ammonium nase activity were subjected to xylanase assay and other precipitation (PY-21%, PF-4.1), anion exchange (PY- characterization studies such as SDS-PAGE, zymography, 31.9%, PF-3) and gel filtration (PY-78.7%, PF-6.6). temperature and pH stability. The SDS-PAGE and zymog - Therefore, ATPS exhibits several advantages over tra - raphy analysis showed the purified enzyme of ~ 85  kDa, ditional purification techniques, i.e., it requires low-cost i.e., endoxylanase (XylB). The purified enzyme was stable materials, low  energy consumption with high yield and in a pH range of pH 6.5 to 7.5 and the temperature range better resolution (Naganagouda and Mulimani 2008; of 20 to 50 °C. The purified enzyme was highly specific to Yasinok et al. 2010; Glyk et al. 2015). The ATPS method is different commercial and natural xylan substrate and has independent of protein concentration and does not affect the potential to generate xylooligosaccharides. the native property of protein (Iqbal et  al. 2016; Ram- akrishnan et al. 2016). Aqueous two‑phase system employed for purification of xylanase Structural properties of xylanase responsible The conventional multistep purification techniques are for thermal and pH stability required for industrial time consuming, which increases the cost of the overall application process and also results in loss of protein at each step The high stability of xylanase was due to the presence (Iqbal et al. 2016; Ramakrishnan et al. 2016). The 60–70% of intrinsic structural properties. The presence of extra of total processing cost in enzyme downstream process disulfide  and salt bridges, hydrophobic side chains, comes from the purification step (Loureiro et  al. 2017; and  N-terminal proline residues helps in  reduction Bhardwaj et  al. 2019). Therefore, several scientists sug - of conformational freedom of the protein structure. u Th s, gested a single step liquid–liquid fractionation technique, it help in providing more stability to protein at the higher Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 18 of 36 Table 4 Purification strategy employed for xylanase from different microorganisms Source organism Purification Specific activity Fold purification Recovery (%) K (mg/mL) V (μmol/mg/ Application of purified enzyme References m max methodology (IU/mg) min) Combined purification strategy Bacillus sp. SV-34S Ammonium sulfate 2803.1 10.62 88.0 3.7 133.33 IU/mL Paper and Pulp industry Mittal et al. (2013) precipitation (80%) Carboxymethyl 3417.2 12.94 13.44 Sephadex C-50 cation exchange chromatography Bacillus sp. GRE7 Ammonium sulfate 191.1 3.9 71 2.23 296.8 IU/mg Eucalyptus kraft pulp bio-bleaching Kiddinamoorthy et al. (40–80%) (2008) DEAE-Cellulose 582.9 11.9 48 Sephadex G-75 1392.6 28.5 27 Arthrobacter sp. Ammonium sulfate 162 2 74 0.9 3571 – Khandeparkar and Bhosle (2006) Sephadex G-200 282.6 3.5 62 DEAE-Sepharose FF 444.2 5.5 49 CM-Sepharose FF 1697.7 21 14 Thermotoga ther- Ni-affinity chroma- 192 6.9 82.3 1.8 769 XOS generation Shi et al. (2014) marum tography Glaeocola mes- Ammonium sulfate 77 9.1 17.4 1.22 98.31 XOS generation, Sea and saline Guo et al. (2009) ophila KMM 241 Dialysis food processing, bakery indus- Ni -NTA Agarose tries resins Streptomyces oliva- Ammonium sulfate 37.35 ± 1.33 1.045 ± 0.002 60.69 ± 2.38 8.16 250.01 High sugar yield and bioethanol Sanjivkumar et al. ceus (MSU3) fractionation generation ability using lignocel- (2017) lulosic biomass Dialysis 82.40 ± 2.50 2.298 ± 0.021 38.29 ± 1.53 DEAE–cellulose 116.98 ± 2.28 3.260 ± 0.024 28.15 ± 1.87 column Sephadex-G-75 153.11 ± 2.11 4.270 ± 0.026 15.57 ± 0.85 column Penicillium gla- Ammonium sulfate 291.78 3.25 84.19 1.2–5.3 212.10–393.17 Purified enzyme suitable for animal Knob et al. (2013) brum fractionation feed additives, clarification, and maceration of juices and wines Molecular exclusion 457.89 5.10 76.92 chromatography (Sephadex G-75 column) Trichoderma Dialysis followed Xyl I-1257.7 Xyl I, II-1.9 Xyl I-62.7 Xyl I-1.6–14.5 Xyl I-462.2–2680.2 XOS generation da Silva et al. (2015) inhamatum by ion exchange Xyl II- Xyl II-3.7 Xyl II-4.0–10.7 U/mg chromatography 1216.4 Xyl II-1972.7–4553.7 (DEAE Sephadex U/mg A-50 column) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 19 of 36 Table 4 (continued) Source organism Purification Specific activity Fold purification Recovery (%) K (mg/mL) V (μmol/mg/ Application of purified enzyme References m max methodology (IU/mg) min) Chrysoporthe Q Sepharose anion – P2-1.2 P2-13.4 P2-1.81 – Efficient saccharification of sugar - de Sousa et al. (2017) cubensis exchange column P3-1.4 P3-1.3 P3-1.18 cane bagasse followed by Sephacryl S-200 gel filtration column Myceliophthora Ni Sepharose resin 102.2 44 7 13.4 ± 1.5 274.5 ± 1.0 Pulp bleaching de Amo et al. (2019) heterothallica containing His- F.2.1.4 Trap HP column Aspergillus flavus Ammonium sulfate 621.4 2.7 46.7 – – Efficiently hydrolyzed pretreated Chen et al. (2019) fractionation corncobs for generation of XOS (40–60%) Gel filtration (HiPrep 838.2 3.7 34.8 16/60 Sephacryl S-100 HR column) chromatography Penicillium chrys- Ion exchange chro- 438.3 9.8 49.3 2.3 mM 731.8 U/mg Beverage, bakery, and feed indus- Terrone et al. (2018) ogenum matography (CM try. For production of xylooligo- Sephadex C-50 saccharides and bioethanol column) Size exclusion 834.2 18.7 31.1 chromatography (Sephadex G-100 column) Single step purification strategy −1 Streptomyces Ammonium sulfate F5-45.44 4.18 F5-60.63 F5-0.2012 F5-0.4742 s Efficient XOS generation Coman et al. (2013) −1 P12-137 precipitation fol- F6-36.48 F6-73.02 F6-0.0388 F6-0.6314 s lowed by dialysis Sorangium cellulo- Ni-affinity followed 4.11 4.03 43.84 38.13 10.69 Hydrolysis of xylan rich substrates Wang et al. (2012) sum So9733-1 by dialysis and and food industries concentration Aspergillus tamarii Single step purifica- 1215.89 7.43 36.72 7.59–8.13 1178.56–1330.20 XOS generation Heinen et al. (2018) Kita tion carboxym- ethyl-cellulose (CM-cellulose) chromatography Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 20 of 36 Table 4 (continued) Source organism Purification Specific activity Fold purification Recovery (%) K (mg/mL) V (μmol/mg/ Application of purified enzyme References m max methodology (IU/mg) min) Scytalidium ther- Ammonium sulfate 125.9 2.5 52 2.4 168.6 IU/mL Agricultural biomass hydrolysis for Kocabacs et al. (2015) mophilum ATCC precipitation application in bioethanol refinery No. 16454 (50%) ATPS (7% Triton 79.8 2.7 79 X-114 top phase) 10 kDa molecular 841.1 4.3 25 weight cut-off (MWCO) Aspergillus oryzae Ammonium sulfate 631 4.1 21 0.2 172.2 XOS generation Bhardwaj et al. (2019) LC1 Precipitation fol- lowed by dialysis Anion exchange 469 3 31.9 Chromatography (DEAE-Sephadex A-50) Gel Filtration 101.5 6.6 78.7 Chromatography (Sepharose G-100) ATPS with Triton 508.9 3.3 69.4 X-114 (5% v/v) ATPS with PEG 2004.3 13 86.8 (22.5% MgSO Salt 11.3% PEG 8000) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 21 of 36 temperature (Turunen et al. 2001; Chen et al. 2015). Dif- respect to volumetric productivity, which suggested that ferent structural modifications such as high Thr/Ser ratio remarkable reduction in cost of enzyme production may and high charged residues, i.e., Arg, cause enhanced be observed under optimized conditions. Thus, based on polar interaction and improved stabilization of the alpha- the above studies, we can suggest that xylanase produc- helix region and secondary structures (Hakulinen et  al. tion can be based on the cost of substrate and consuma- 2003). The xylanase protein has a large number of ion ble, along with the cost of each step involved in upstream pairs/aromatic residues on the surface of protein result- and downstream processing. Therefore, utilizing cheap ing in enhanced interactions (Polizeli et  al. 2005; Chen raw materials, less number of steps during upstream et  al. 2015). The low average protein rigidity i.e. low B and downstream process (such as single step purifica - factor, low flexibility results in  high rigidity at extreme tion instead of multistep process) can help in keeping the physical conditions (Xie et  al. 2014). The presence of enzyme production cost as low as possible. divalent metal ions and removal of N or C terminal dis- ordered residues protect xylanase from heat and protease Xylanase employed as a greener tool in different inactivation (Andrews et al. 2004; Chen et al. 2015). The industries presence of carbohydrate-binding modules (CBM22 and Xylanase with such unique characteristics of thermo- CBM9) at N or C terminal often imparts heat stabil- alkali tolerant nature has a diverse range of application ity to xylanase. The pH stability of the xylanases is often in different industries such as paper and pulp, deinking, affected by the presence of several amino acids near the biomass utilization and food feed industries (Fig. 6). catalytic residues (Singh et al. 2019). Xylanase employed in the food and feed industry Cost estimation of the xylanase production Bakery Polizeli et al. (2005) suggested that 20% of the total global The xylanase finds application in food industries such enzyme production is from biomass hydrolysis enzymes, as bakery. The bread is made up of wheat consisting i.e., xylanase, cellulase and pectinases. An extensive of hemicelluloses such as arabinoxylan. The xylanase study on cost involved in each step of xylanase produc- can solubilize the water unextractable arabinoxylan tion at industrial scale is unavailable on public domain. into water-extractable arabinoxylan (Courtin and Del- Klein-Marcuschamer et  al. (2012) performed a study on cour 2002). This help in uniform water distribution and the cost analysis of application of enzymes during the lig- improvement in gluten network formation throughout nocellulosic biomass based biofuel production and sug- the dough. The addition of xylanase improves the rheo - gested breakdown of the operating cost (annual) in their logical properties of dough such as softness, extensibil- enzyme production facility. They suggested percentage ity, and elasticity along with bread-specific volume and of cost involved for each component, i.e., raw materials crumb firmness (Harbak and Thygesen 2002; Camacho (28%), labor (7%), transportation (1%), consumables (4%), and Aguilar 2003; Butt et al. 2008). The breakdown prod - utilities (10%), facility dependent (48%), and waste treat- ucts of arabinoxylan, i.e., arabino-xylooligosaccharides in ment (2%). This clearly shows that maximum contribu - bread have its health benefits (Polizeli et al. 2005; Bajpai tion of 48% comes from the capital investment followed 2014). by cost of substrate (28%). Klein-Marcuschamer et  al. Butt et  al. (2008) demonstrated the role of GH11 (2012) also suggested the baseline production cost of endoxylanases from B. subtilis in solubilizing the ara- hydrolysis enzyme as $10.14/kg. binoxylan. This increases the viscosity and volume of Da Gama Ferreira et al. (2018) performed techno-eco- dough and decreases gluten agglomeration and dough nomic analysis of the β-glucosidase enzyme production firmness resulting in the development of uniform and from E. coli on industrial scale. They showed  major cost fine crumbs. GH11 xylanase (0.12 U/g flour) from Peni - during industrial production are facility dependent (45%) cillium occitanis Pol6 resulted in improvement of bread- followed by raw materials (25%) and consumables (23%), making process such as the decrease in water absorption that  are similar to observations made by  Klein-Marcus- (8%) and an increase in dough rising (36.8%), volume chamer et al. (2012). Capital investment/facility-depend- (17.8%), specific volume (34.9%) and cohesiveness. The ent cost is required for development of infrastructure bread has improved rheological and sensory properties (i.e., equipments), insurance, maintenance and depre- (texture, taste, flavor, softness, and overall acceptability). ciation. This upstream and downstream process during Low springiness and gumminess were observed in the enzyme production involves the cost on part of capital bread prepared using xylanase (Driss et al. 2013). Partially investment along with the cost of consumables and utili- purified microbial xylanase was used by Ghoshal et  al. ties. da Gama Ferreira et  al. (2018) performed sensitiv- (2013) to produce whole‐wheat bread with better sen- ity analyses of process scale, inoculation volume with sory properties (brighter color). The addition of xylanase Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 22 of 36 Fig. 6 Xylanase as a greener tool in different industries also resulted in increased specific volume, and shelf life, Streptomyces sp was used for the clarification of orange, with lower firmness and reduced staling during storage. mousambi, and pineapple with 20.9%, 23.6% and 27.9% Panzea, new generation xylanase obtained from Bacillus clarity, respectively (Rosmine et  al. 2017). Immobilized Licheniformis, can help in improving dough properties at xylanase obtained from Bacillus pumilus VLK-1 was low enzyme dosage. It helps in achieving the desired tex- used for orange (29%) and grape juice (26%) enrichment ture, appearance, loaf volume and crumb structure (Baj- (Kumar et  al. 2014). Xylanase immobilized on 1,3,5-tri- pai 2014). Similarly, recombinant xylanase (r-XynBS27) azine-functionalized silica-encapsulated magnetic nano- obtained from Pichia pastoris (xynBS27 gene from Strep- particles was reported to clarify the three different types tomyces sp. S27) used as an additive during bread-making of fruit juices after five hours of incubation at 50  °C process. The recombinant xylanase resulted in improve - (Shahrestani et al. 2016). Partially purified xylanase from ment in a specific volume and reducing sugar content Streptomyces sp AOA40 was used in fruit juice industry with a decrease in firmness, consistency, and stiffness (De for increased clarity of juices from apple (17.8%), orange Queiroz Brito Cunha et al. 2018a, b). (18.4%) and grape (17.9%) (Adigüzel and Tunçer 2016). Glutaraldehyde-activated immobilized xylanase was Fruit juice clarification used for the clarification of tomato juice. Xylanase from The enzymatic process in fruit juice extraction and clari - P. acidilactici GC25 was used to treat the kiwi, apple, fication is widely used. Raw juices of fruit contain poly - peach, orange, apricot, grape, and pomegranate in which saccharides such as cellulose, hemicellulose, starch pectin increase in the amount of reducing sugar was observed and surface-bound lignin and decrease the quality of the along with the decrease in turbidity of the juice (Adiguzel juice, e.g., hazy color and high viscosity (Danalache et al. et al. 2019). 2018). The use of enzymes decreases the viscosity and avoids the formation of clusters, by removing the sus- Animal feed pended and undissolved solid using centrifugation and Xylanases plays an important role in animal feed by filtration methods. This increases the clarity, aroma, and breaking the feed ingredient arabinoxylan and reduces color of the juice (Danalache et  al. 2018). Xylanase from the raw material viscosity. Aspergillus japonicus C03 with Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 23 of 36 good endoxylanase and cellulase production ability with xylanase using agro-residues active at high temperature high stability in the presence of goat ruminal environ- 60 °C and pH 6–10 and was utilized for bio-bleaching of ment showed ruminant feed applications (Facchini et  al. kraft pulp (Azeri et  al. 2010). Paenibacillus campinasen- 2011). A number of studies reported the availability of sis BL11 xylanase pretreatments showed the increased distillers dried grains with soluble (DDGS) to be utilized brightness and viscosity of hardwood kraft pulp (Ko et al. in animal feeds and use of exogenous xylanase in poul- 2010). S. thermophilum xylanase active at high tempera- try diets to treat the higher fiber content (Pirgozliev et al. ture (50–70  °C) was used for the bleaching of bagasse 2016; Whiting et al. 2019). The exogenous enzymes effec - pulp (Joshi and Khare 2011). T. lanuginosus VAPS24 tively improved the nutritional value of co-products of xylanase was stable at wide range pH that can be use- bioethanol as reported previously with DDGS obtained ful in both alkaline and acidic bioprocesses (Kumar and from corn (Liu et al. 2011). Xylanases have been involved Shukla 2018). An alkaliphilic Bacillus liceniformis Alk-1 in animal feed over decades, as it reduces the viscos- xylanase was utilized in a purified form for the enzy - ity of digesta in poultry. Xylanase addition showed the matic pretreatment on eucalyptus kraft pulp bleach- weight gain improvement and enhanced feed conver- ing (Raj et  al. 2018). The xylanase preparation obtained sion ratio because of the improvement in the arabinoxy- from white-rot fungi, S. commune ARC-11 was capable of lan digestibility in monogastric animal diets (Paloheimo ethanol soda pulp pre-bleaching from Eulaliopsisbinata et  al. 2010; Van Dorn et  al. 2018). Xylanase utilized as a (Gautam et  al. 2018). The paper  manufacturing units dietary supplement for the nutrients digestibility, digesta of various countries, i.e., Japan. South America, North viscosity growing pigs fed corn intestinal morphology America and Europe are slowly replacing chemical pulp diet based on soybean meal was reported by Passos et al. bleaching by xylanase mediated pulp bleaching. Canada (2015). ECONASE XT a well-known commercial endo- is known to be the leading producer of pulp and they are 1,4-β-xylanase which has been used as feed additives for bleaching more than 10% its pulp via xylanase (Dhiman chicken fattening, weaned piglets and fattening for pigs et al. 2008a). In addition to that, several reports also sug- (Rychen et al. 2018). gest that the xylanase enzyme-mediated pretreatment can help in generation of cellulosic nanofibres (CNF) Xylanase in paper and pulp industries with improved crystallinity from unbleached bagasse and Bio‑bleaching eucalyptus pulp (Nie et  al. 2018; Zhang et  al. 2018; Tao The process of removal of lignin from wood pulp to et  al. 2019). Zhang et  al. (2018) suggested that applica- produce bright and completely white finished paper tion of commercial Novozyme X2753 can simplify the is known as bleaching (Beg et  al. 2001). Traditionally, CNF’s production and purification process. Tao et  al. chemical bleaching agents (such as chlorine) were used (2019) demonstrated that xylanase can directly act on for bleaching (Subramaniyan and Prema 2002). The use the unbleached pulp, where it acts on the covalent bond of ligno-hemicellulolytic enzymes for bleaching has between hemicellulose molecule and hydrogen bond gained impetuous all over the world. Xylanases are capa- between hemicelluloses and cellulose. The presence of a ble of hydrolyzing xylan which is linked to the cellulose small amount of hemicelluloses in cellulose nanofibrils and lignin of the pulp fiber. Thus, xylan disruption will increases light blockage efficiency and subsequently the eventually lead to the separation between these compo- energy storage capacity of solar cells. Thus, xylanase- nents, enhance swelling in the fiber wall, and improve mediated bio-bleached pulp acts as a potential substrate lignin extraction from the pulp (Thomas et  al. 2015). for flexible solar cells. uTh s, xylanase in combination with lignin-degrading enzyme help in increasing the brightness of pulp (Vii- Deinking of waste paper kari et al. 1994; Sunna and Antranikian 1997; Pérez et al. The dislodgement of ink from the waste used paper is 2002; Motta et  al. 2013). The exposures of the cellulose required for its recycling and reuse. Chemical-based fiber to enzymatic pulping enhance the bonding forces methods involving chlorine or chlorine-based deriva- of paper and improve paper strength via degradation of tives, ClO , NaOH, NaCO, H O, Na SiO , have been 3 2 2 2 2 xylan and removal of lignin during enzymatic treatment used for removing ink from the paper. This resulted in (Lin et  al. 2018). The enzymatic system has been highly generation of hazardous effluents and required tedious selective, non-toxic, environmentally friendly approach treatment before disposal to the environment (Maity for bio-bleaching (Bajpai 2012). et  al. 2012). The enzyme-based methods utilizing xyla - Paper and biomass pulp processing takes place at vary- nase and laccase have been suggested for the removal of ing pH and temperature. Therefore, thermo-alkali stable ink from paper and pulp industries effluents (Chandra xylanases are required for the bio-bleaching. An alkaliph- and Singh 2012; Dhiman et al. 2014). ilic Bacillus strain produced thermoactive cellulase-free Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 24 of 36 Virk et  al. (2013) explored the deinking efficiencies of Garg et  al. (2013) demonstrated the application of bacterial alkalophilic laccase and xylanase along with alkalo-thermostable xylanase from Bacillus pumilus ASH physical deinking methods such as microwave and ultra- in bioscouring of jute fabric. The oven-dried jute fabric sound for recycling of waste paper. The combination of when incubated with a small dose of 5  IU/g xylanase at xylanase and laccase enzymes showed an increase in 55  °C for 2  h resulted in an increase in 4.3% whiteness brightness of different waste pulp old newsprint pulp and 10.7% brightness of fabric. Further, it also helped in (21.6%), inkjet print pulp (4.1%), laser print pulp (3.1%), decreasing in yellowness of fabric by 5.57%. Similarly, magazine pulp (8.3%), and xerox paper pulp (1.9%) only. xylanase from Bacillus pumilus was studied for enzy- Gupta et  al. (2015) reported that synergistic action matic desizing of cotton and micropoly fabrics (Battan of xylanase and laccase enzyme (co-cultivation of Bacillus et al. 2012). The enzymatic desizing with enzyme load of sp. and B. halodurans FNP135) resulted in improvement 5  IU/g at pH 7.0, temperature 60  °C for 90  min resulted of physical properties like freeness, breaking length, burst in improved whiteness of 0.9% with respect to the chemi- factor and tear factor by 17.8%, 34.8%, 2.77%, and 2.4%, cal process. The addition of surfactant such as EDTA respectively, of old newspaper. The appearance of the improved the desizing and bioscouring efficiency (Loson - newspaper was also improved with an increase in 11.8% czi et al. 2005; Battan et al. 2012; Garg et al. 2013). brightness and 39% whiteness. The effective dose of com - The synergistic action of xylanase and pectinase mercial cellulase and xylanase from Bacillus halodurans enzyme was used for scouring of cotton fabrics. The bios - TSEV1 for removal of ink was determined at 1.2. U/mg couring was performed with 5.0  IU xylanase and 4.0  IU (each enzyme) by Kumar and Satyanarayana (2014). The pectinase from Bacillus pumilus  strain AJK (MTCC cellulase and xylanase complex obtained from Escheri- 10414) along with surfactants such as 1.0  mM EDTA chia coli SD5 facilitated the reduction in hexenuronic and 1% Tween-80 at high pH 8.5 for 1  h at 50  °C. They acid (Hex A) and kappa number, increase in brightness observed improvement in whiteness, brightness, and (10%) and tear strength of recycled paper (Kumar et  al. reduction in yellowness by 1.2%, 3.2%, and  4.2% respec- 2018c). tively  that is better  in comparison to chemical-based alkaline scouring method (Singh et  al. 2018). El et  al. (2018) reported improvement in desizing, bioscouring Xylanase employed in textile industries and bio-finishing efficiency using xylanase obtained from The textile processing can be broadly divided into desiz - T. longibrachiatum KT693225 without any requirement ing, scouring and bleaching. Desizing involves removal of additives. of adhesive material from plant fibers and scouring to remove the inhibitory material from desized fibers Xylanase employed in chemical (Hartzell et  al. 1998; Dhiman et  al. 2008b). The conven - and pharmaceutical industries tional method used for desizing and scouring involves The non-digestible sugar molecules together form oli - the application of high temperature under the influence gomers known as xylooligosaccharides, which are made of oxidizing agents in the alkaline system. This method up of xylose monomers (Vazquez et  al. 2000). XOS has is not only chemical intensive but also non-specific that various applications in biotechnology, pharmaceuti- causes hamper to the useful cellulosic fractions compro- cal, food and feed industries (Chang et  al. 2017). XOS mising the overall strength of the textile fibers. Therefore, plays a vital role as prebiotic as it is not hydrolyzed application of highly thermo-alkali stable cellulase-free or absorbed in the gastrointestinal tract. uTh s, XOS xylanolytic enzyme can efficiently be used for desizing selectively stimulates the growth of important gastro- and scouring (Csiszár et  al. 2001; Losonczi et  al. 2005; intestinal microorganisms regulating the human diges- Dhiman et al. 2008b; Bajpai 2014). tive health (Roberfroid 1997; Collins and Gibson 1999; Dhiman et al. (2008b) demonstrated the application of Vazquez et al. 2000). The potential of XOS as an efficient alkalo-thermophilic xylanase from Bacillus stearothermo- feed alternative is established by the fact that it  help in philus SDX for processing of cotton and microply fabrics. cholesterol reduction, inhibit starch retro-gradation, The desizing and bioscouring treatments were performed improve the bioavailability of calcium thus improving using 5 g/L of xylanase at 70 °C, pH 9.5, for 90 min. This the nutritional and sensory properties of food (Voragen resulted in weight loss for 0.91% in microply and 0.83% 1998; Motta et al. 2013). XOS has shown the application in cotton with overall whiteness index of 11.81% for cot- in pharmaceutical sectors due to its immunomodulatory ton and 52.15% for micropoly. The processed fabric has (Chen et  al. 2012), anti-cancerous (Gupta et  al. 2018), increased tensile strength (1.1–1.2%) and tearness value anti-microbial, antioxidant (Kallel et  al. 2015b), anti- (1.6–2.4%) as compared to control. allergy, anti-inflammatory (Aachary and Prapulla 2011), Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 25 of 36 and anti-hyperlipidemic activity (Li et  al. 2010). XOS hydrolysis of the pretreated biomass for the conversion have also shown phyto-pharmaceutical and feed applica- of complex carbohydrate polymer of LCB to the simple tions such as growth regulatory activity in aquaculture monomers which will be further converted to ethanol by and poultry. These properties may be due to the presence fermentation. The xylanolytic enzyme in combination of uronic substituents in acidic oligosaccharides. with cellulolytic enzyme plays an important role in the The process of XOS synthesis involves the physi - hydrolysis process. cal (autohydrolysis), chemical (hydronium ions gener- Several reports suggest that xylanase obtained from sev- ated by water autoionization and in  situ organic acids) eral microorganisms plays an important role in sacchari- or enzymatic hydrolysis (xylanase or β-xylosidase) of fication of LCB for lignocellulosic-based biorefinery (Hu hemicellulose-rich agricultural wastes (Aachary and et  al. 2011; Choudhary et  al. 2014; Ramanjaneyulu et  al. Prapulla 2011). Several reports suggested that XOS can 2017; Basit et  al. 2018). Hydrolysis and fermentation are be enzymatically produced from different agro-residues important steps in biomass to bioethanol generation. Ini- such as hardwoods (Huang et  al. 2016), straws (Gullón tially, several groups demonstrated separate hydrolysis of et  al. 2008; Kallel et  al. 2015a; Moniz et  al. 2016) corn biomass followed by fermentation (SHF). SHF is a time- cobs (Chapla et  al. 2013; Gowdhaman and Ponnusami consuming process and thus increases the overall cost of the 2015), bran (Otieno and Ahring 2012), sugarcane bagasse process. Later on, different integrated process (combined (Jayapal et al. 2013) and bamboo (Xiao et al. 2013) using hydrolysis and fermentation) have been developed such as microbial xylanases. simultaneous saccharification and co-fermentation (SSCF), Alkaline xylanase from Bacillus mojavensis A21 utilized simultaneous saccharification and fermentation (SSF), and corncob xylan for the release of xylotriose and xylobiose consolidated bioprocessing (CB) (Malhotra and Chapad- (Haddar et  al. 2012). Bacillus aerophilus KGJ2 xylanase gaonkar 2018). These strategies resulted in an enhancement showed efficiency toward XOS synthesis, e.g., xylobiose, in reaction rates and ethanol yields (Eklund and Zacchi xylotriose, and xylose after hydrolysis of xylan (Gowdha- 1995; Sun and Cheng 2002). Bibra et  al. (2018) showed man et  al. 2014). A cellulase free xylanase (EX624) from thermostable xylanase production using Geobacillus sp. Streptomyces sp. CS624 produced xylose, xylobiose and DUSELR13, which is applied further for ethanol generation xylotriose with commercial beech wood xylan and wheat from LCB. SSF Geobacillus sp. DUSELR13 and Geobacillus bran (Mander et al. 2014). Using deoiled Jatropha curcas thermoglucosidasius are co-cultured for SSF of prairie cord seed cake as substrate, Sporotrichum thermophile xyla- grass (PCG), and corn stover (CS). The SSF resulted in 3.53 nase was produced which showed the efficiency to pro - and 3.72 g/L ethanol from PCG and CS, respectively. duce XOS by the hydrolysis of oat spelt xylan, with 73% Hu et  al. (2011) suggested that xylanase causes fiber xylotetraose, 15.4% xylotriose and 10% xylobiose (Sadaf swelling improving porosity that helps in improving and Khare 2014). Xylanase obtained from the mixed the accessibility of cellulose. To ferment both cellulose- microbial culture of Cellulomonas uda NCIM 2523 and derived hexoses (C6) and xylan-derived pentoses (C5), Acetobacter xylinum NCIM 2526 using Prosopis juliflora simultaneous saccharification and co-fermentation showed the potential to produce XOS with probiotic (SSCF) was introduced which causes ethanol production activity from beech wood xylan (Anthony et  al. 2016). using single microorganisms co-cultured with cellulase A xylanase gene PbXyn10A isolated from Paenibacil- and xylanase producing strain. Yasuda et al. (2014) dem- lus barengoltaii cloned in E. coli showed 75% XOS yield onstrated bioethanol generation by SSCF of anhydrous from xylan extracted from raw corncobs (Liu et al. 2018). ammonia-pretreated  Pennisetum purpureum Schumach The hydrolysis of xylan using xylanase from Pichia stipitis (Napier grass) using Escherichia coli KO11 and Saccha- produced 2% XOS consisting of xylotetraose 14%, xylotri- romyces cerevisiae cellulase, and xylanase. SSCF for 96 h ose 49% and xylobiose 29% (Ding et  al. 2018). Bhardwaj was reported to have a maximum 74% ethanol yield as et al. (2019) demonstrated the partially purified xylanase compared to theoretical yield calculated based on glucan obtained from Aspergillus oryzae LC1 resulted in the and xylan yield of 397 mg/g and 214 mg/g, respectively. generation of xylobiose, xylotriose, and xylotetraose. Bondesson and Galbe (2016) designed experimen- tal setup of SSCF for ethanol production from steam- Xylanase employed in biorefinery pretreated, acetic acid-impregnated wheat straw using Efficient conversion of lignocellulosic biomass (LCB) into a pentose fermenting S. cerevisiae KE6-12b strain. The fuel-grade ethanol has become a world priority for pro- highest 37.5  g/L ethanol concentration with 0.32  g/g ducing environmentally friendly renewable energy at a ethanol yield was obtained based on the glucose–xylose reasonable price for the transportation sector. The pro - available in the pretreated wheat straw. Shariq and Sohail cess of bioconversion of lignocellulosic biomass requires (2018) demonstrated that yeast strain Candida tropicalis Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 26 of 36 MK-160 can help in xylanase and endoglucanase produc- having ligno-hemicellulolytic enzymes having the capa- tion as well as ethanol production. Therefore, it can be bility along with ethanol generating potential. Shen et al. potentially used for SSCF involves single microorganism. (2012) engineered a thermostable self-splicing bacterial The consolidated processing or simultaneous deligni - intein-modified xylanase for consolidated lignocellu - fication, saccharification, and fermentation involve the losic biomass processing. Sun et al. (2012) demonstrated cultivation of ligno-hemicellulolytic enzyme-producing expression of recombinant Saccharomyces cerevisiae strains along with ethanol-producing strain in a reactor. strain having an engineered minihemicellulosome. It It may be monoculture or co-culture of different microor - has the capability of converting xylan directly to ethanol. ganisms. It will help to decrease the overall process cost Horisawa et  al. (2019) suggested direct ethanol produc- required for bioreactor and operation of different enzyme tion from lignocellulosic materials by consolidated bio- production and ethanol generation (Chadha et al. 1995). processing using the mixed culture of wood rot fungi, i.e., To design a monoculture-based consolidated pro- Schizophyllum commune, Bjerkandera adusta, and Fomi- cessing, different engineered microorganisms are used topsis palustris. Fig. 7 Future prospect for development in area of xylanase production using conventional and advanced approaches Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 27 of 36 Commercial xylanase enzyme and their application bioinformatics tools to develop different approaches for The xylanase enzyme is commercially employed in sev - enhanced xylanase production. The combination of new eral industries such as pulp bleaching, food, feed, and technology such as synthetic biology (DNA oligo-synthe- brewing. The major application of the xylanase is in pulp sis) and conventional recombinant DNA technology can bleaching and is produced by different companies around be used for attaining the objective of high xylanase pro- the world with various trade name such as Bleachzyme duction with desired industrial properties (Fig.  7). How- (Biocon, India), Cartzyme (Sandoz, US), Cartzyme MP ever, limitations associated with mimicking the natural (Clarient, UK), Ecozyme (Thomas Swan, UK), Irgazyme system into synthetic system need to be taken care before 10 A & Irgazyme 40–4× (Genercor, Finland), Ecopulp full-scale applications. Also, the ethical, socio-economic (Alko Rajamaki, Finland), VAI Xylanase (Voest Alpine, and health concerns need to taken care before  commer- Austria), and Rholase 7118 (Rohm, Germany). Xylanase cial exploitation of the developed strategies. is commercially produced by several international indus- tries for its application in food and feed industries. San- Conclusion kyo from Japan, Ciba Giegy from Switzerland produces The enzymatic breakdown of the xylan into its constitu - xylanase as trade name Sanzyme, and Albazyme-10A, ent component requires the synergistic action of xyla- respectively, and has been used commercially in food and nases and other debranching enzymes. The key enzyme baking industries. A Danish firm Novo Nordisk, produces used for xylan hydrolysis is endo-1,4-β-xylanase that three commercial xylanases namely Pulpzyme (HA, HB, cleaves β-1,4-glycoside linkage of xylan. The xylanase HC), Biofeed (Beta, plus) and Ceremix and used in pulp can be grouped under different GH families with major bleaching, feed and brewing industries, respectively xylanases from GH10 or GH11 families, followed by (Walia et al. 2017). An American firm Alltech, Inc., com - GH5, GH7, GH8 and GH43. The xylanase enzyme acts mercially produces xylanase with trade name Allzym PT as a “Green” alternative to already existing industrial and Fibrozyme and has been used for the upgrading the processes for processing of xylan to different industrially animal feed. A Japanese firm named Amano Pharmaceu - important product such as paper, textile, food, feed, phar- tical Co, Ltd. produced xylanase enzyme named Amano maceuticals, and biofuels. The application of xylanases 90 and it has been used in food, feed and pharmaceuti- in the production of the above-mentioned products can cal industries. Most of the commercial xylanases are regulate the overall economics of the process. Therefore, produced by fungal source due to its high production already existing method can be further improved or new potential. strategies may be developed for enhanced and cost-effi - cient production of xylanase with desired characteristics. Further, it is often observed that native enzyme cannot Challenges and future trends in commercial meet the industrial process requirement; thus, the com- production, purification and application bination of already existing technology with new tech- of xylanase nology such as synthetic biology (DNA oligo-synthesis), The search of super xylanase is still on, therefore, search - rational engineering and directed evolution can be used ing for new microbial source with the ability to produce for attaining the objective of high xylanase production highly active and stable xylanase is going on around the with desired industrial properties. world. The strains isolated from different extreme habitat can be of potential applications as these strains already possesses the ability to withstand different stress such Abbreviations as high temperature and pH variations. The selection LCB: lignocellulosic biomass; EC: enzyme commission; HMWLI: high-molecular weight with low isoelectric point; LMWHI: low-molecular weight with high of such thermal and pH tolerant strains and subjecting isoelectric point; CAZy: carbohydrate-active enzyme database; NCBI: National them to different optimization strategies for enhanced Centre for Biotechnological Information; GH: glycoside hydrolase; XOS: xylo- xylanase production can be one alternative. The advance oligosaccharides; X2: xylobiose; X3: xylotriose; X4: xylotetraose; CNB: catalytic nucleophile/base; CPD: catalystic proton donor; Asp: aspartic acid; Glu: gluc- ment in biotechnological tools and techniques (Recom- tamic acid; SmF: submerged fermentation; SSF: solid-state fermentation; CMC: binant DNA technology or genetic engineering) provides carboxymethyl cellulose; OFAT: one factor at a time; CCD: central composite an opportunity to select the gene responsible for xylanase design; ANOVA: analysis of variance; RSM: response surface methodology; GRAS: generally regarded as safe; TCA: tr ichloroacetic acid; SDS–PAGE: sodium production that can be isolated and efficiently transferred dodecyl sulfate-polyacrylamide gel electrophoresis; DEAE: diethylaminoethyl; to the expression system. These expression systems can FPLC: fast protein liquid chromatography; ATPS: aqueous two-phase system; be regulated for enhanced production of xylanase with PEG: polyethylene glycol; DDGS: distillers dried grains with soluble; SSCF: simultaneous saccharification and co-fermentation; SSF: simultaneous sac- desired property for specific industrial applications. The charification and fermentation; CB: consolidated bioprocessing; PCG: prairie availability of a high amount of genomics, proteom cord grass; CS: corn stover. ics and metabolomics data can be used via different Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 28 of 36 Acknowledgements Ahmed S, Riaz S, Jamil A (2009) Molecular cloning of fungal xylanases: an The authors are thankful to the Department of Biotechnology, Government of overview. Appl Microbiol Biotechnol 84:19–35 India for providing the financial support (Grant Nos. BT/304/NE/TBP/2012 and Akila G, Chandra TS (2003) A novel cold-tolerant Clostridium strain PXYL1 BT/PR7333/PBD/26/373/2012). NB is thankful to the University Grants Commis- isolated from a psychrophilic cattle manure digester that secretes ther- sion for providing fellowship for doctoral studies. BK is thankful to Jawaharlal molabile xylanase and cellulase. FEMS Microbiol Lett 219:63–67 Nehru memorial Fund and CSIR for providing scholarship for doctoral studies. Al Balaa B, Wouters J, Dogne S et al (2006) Identification, cloning, and expression of the Scytalidium acidophilum XYL1 gene encoding for an Authors’ contributions acidophilic xylanase. Biosci Biotechnol Biochem 70:269–272. https :// NB and BK developed the manuscript and wrote the manuscript under guid- doi.org/10.1271/bbb.70.269 ance of PV. PV provided time to time scientific and technical comments to Alam M, Gomes I, Mohiuddin G, Hoq MM (1994) Production and characteriza- enhance the quality of manuscript. All authors read and approved the final tion of thermostable xylanases by Thermomyces lanuginosus and Ther- manuscript moascus aurantiacus grown on lignocelluloses. Enzyme Microb Technol 16:298–302. https ://doi.org/10.1016/0141-0229(94)90170 -8 Funding Amore A, Parameswaran B, Kumar R et al (2015) Application of a new xylanase The authors thank Department of Biotechnology, Government of India (Grant activity from Bacillus amyloliquefaciens XR44A in brewer’s spent grain Nos. BT/304/NE/TBP/2012 and BT/PR7333/PBD/26/373/2012). saccharification. J Chem Technol Biotechnol 90:573–581. https ://doi. org/10.1002/jctb.4589 Availability of data and materials Andrews SR, Taylor EJ, Pell G et al (2004) The use of forced protein evolution to Not applicable. investigate and improve stability of family 10 xylanases the production of Ca2 -independent stable xylanases. J Biol Chem 279:54369–54379 Ethics approval and consent to participate Ang SK, Ariyani LP et al (2013) Production of cellulases and xylanase by Asper- Not applicable. gillus fumigatus SK1 using untreated oil palm trunk through solid state fermentation. Process Biochem 48:1293–1302. https ://doi.org/10.1016/j. Consent for publicationprocb io.2013.06.019 Not applicable. Anthony P, Harish BS, Jampala P et al (2016) Statistical optimization, purifica- tion and applications of xylanase produced from mixed bacteria in Competing interests a solid liquid fermentation using Prosopis juliflora. Biocatal Agric The authors declare that they have no competing interests. Biotechnol 8:213–220 Azeri C, Tamer UA, Oskay M (2010) Thermoactive cellulase-free xylanase pro- Received: 18 July 2019 Accepted: 9 October 2019 duction from alkaliphilic Bacillus strains using various agro-residues and their potential in biobleaching of kraft pulp. 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A detailed overview of xylanases: an emerging biomolecule for current and future prospective

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Copyright © 2019 by The Author(s)
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Chemistry; Biochemical Engineering; Environmental Engineering/Biotechnology; Industrial and Production Engineering
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10.1186/s40643-019-0276-2
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Abstract

Xylan is the second most abundant naturally occurring renewable polysaccharide available on earth. It is a complex heteropolysaccharide consisting of different monosaccharides such as l -arabinose, d -galactose, d -mannoses and organic acids such as acetic acid, ferulic acid, glucuronic acid interwoven together with help of glycosidic and ester bonds. The breakdown of xylan is restricted due to its heterogeneous nature and it can be overcome by xylanases which are capable of cleaving the heterogeneous β-1,4-glycoside linkage. Xylanases are abundantly present in nature (e.g., molluscs, insects and microorganisms) and several microorganisms such as bacteria, fungi, yeast, and algae are used extensively for its production. Microbial xylanases show varying substrate specificities and biochemical proper - ties which makes it suitable for various applications in industrial and biotechnological sectors. The suitability of xyla- nases for its application in food and feed, paper and pulp, textile, pharmaceuticals, and lignocellulosic biorefinery has led to an increase in demand of xylanases globally. The present review gives an insight of using microbial xylanases as an “Emerging Green Tool” along with its current status and future prospective. Keywords: Xylan, Xylanase, Glycoside hydrolase, Green tool Introduction covers 33% of total lignocellulosic biomass found on the The major constituent of the plant cell wall is “lignocellu - globe (Collins et al. 2005; Polizeli et al. 2005; Chávez et al. loses”, as the name suggests it consists of lignin (15–20%), 2006; Walia et al. 2017). It accounts for 15–30% in hard- hemicellulose (25–30%) and cellulose (40–50%) (Gray woods and 7–10% in softwood (Walia et al. 2017). There et al. 2006; Singla et al. 2012). These components together is a need for depolymerization of this complex polymer form a three-dimensional complex network with the for its efficient utilization in different industrial applica - help of covalent and non-covalent interactions (Sánchez tion. Xylanase is a group of enzymes consisting of endo- 2009). Hemicelluloses consist of xylan, a heteropolysac- 1,4-β-d-xylanases (EC 3.2.1.8), β-d-xylosidases (E.C. charide substituted with monosaccharides such as l-ara - 3.2.1.37), α-glucuronidase (EC 3.2.1.139) acetylxylan binose, d-galactose, d-mannoses and organic acids such esterase (EC 3.1.1.72), α-l-arabinofuranosidases (E.C. as acetic acid, ferulic acid, glucuronic acid interwoven 3.2.1.55), p-coumaric esterase (3.1.1.B10) and ferulic acid together with help of glycosidic and ester bonds (Collins esterase (EC 3.1.1.73) involved in the depolymerization et al. 2005; Ahmed et al. 2007; Motta et al. 2013; Sharma of xylan into simple monosaccharide and xylooligosac- 2017). Xylan is readily available in nature, followed by cel- charides (Gomez et al. 2008; Juturu and Wu 2014; Walia lulose the second most abundant polysaccharide which et al. 2017; Romero-Fernández et al. 2018). Xylanases are produced by different living organisms such as microorganisms, protozoans, and molluscs, and *Correspondence: vermaprad@yahoo.com; pradeepverma@curaj.ac.in also  found in the rumen of higher animals (Beg et  al. Nisha Bhardwaj and Bikash Kumar contributed equally to this work 2001). The xylanases are mainly produced by micro - Bioprocess and Bioenergy Laboratory, Department of Microbiology, organisms, e.g., bacteria, fungi, and actinomycetes at Central University of Rajasthan, NH-8, Bandarsindri, Kishangarh, Ajmer 305817, India © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 2 of 36 industrial scale (Motta et al. 2013). The utilization of lig - glucopyranosyl, 4-O-methyl-d-glucuronopyranosyl, nocellulosic biomass (LCB) for production of different p-coumaroyl or α-l-arabinofuranosyl side-chain groups biochemicals such as bioethanol, enzymes, and value- with varying degrees. Xylanolytic enzymes play a key added compounds has tremendously improved in recent role in the breakdown of the complex structure of xylan. years. It results in providing opportunities for scientists Hence, for complete and efficient hydrolysis of xylan to explore the hydrolytic potential of xylanase for effi - into its constituent sugars requires synergistic action of cient saccharification of LCB for ethanol and xylooligo - various enzymes with specifically targeting appropriate saccharides generation. Xylanase also finds application bonds of xylan. in several industries like pulp and paper bleaching, food, The multifunction xylanolytic system exists in bacte - feed, and pharmaceuticals. ria (Zhang et  al. 2016a, 2016b), fungi (Driss et  al. 2011; Xylanase is required in huge amount for industrial Bhardwaj et  al. 2018) and actinomycetes (Hunt et  al. level application with characteristic properties to survive 2016) where xylan backbone is randomly cleaved by the harsh industrial level processing’s (Qiu et  al. 2010). the action of endo-1,4-β-d-xylanases; xylose polymer is Therefore, there is a need to select potent microorgan - broken down to its monomeric form by action of β-d- isms for xylanase production, followed by optimization of xylosidases. Acetyl and phenolic side branches were media components for enhanced production. The under - removed by the action of α-glucuronidase and acetylxy- standing of the genetic constituents of the microbe will lan esterase. α-l-Arabinofuranosidases catalyze the help in deducing the mode of action of the enzyme. This removal of the side groups. The ester bonds present on will help in regulating the enzyme action for employment the xylan are cleaved by the action of p-coumaric ester- in desired industrial application. The microorganisms ase and ferulic acid esterase (Beg et  al. 2001; Collins also produce other protein and metabolites with desired et  al. 2005; Chakdar et  al. 2016; Walia et  al. 2017). The xylanase enzyme. Therefore, purification of the crude schematic structure of xylan showing bonds which are enzyme is a prerequisite to obtain purified enzymes. The attacked by a specific xylanolytic enzyme for complete characterization of purified xylanase will help in elucidat - hydrolysis of xylan to its constituent monomeric units is ing its stability and specificity toward different substrates. represented in Fig. 1. This will help in selecting the suitable industrial process in which it can be utilized. With the advent of advanced Classification of xylanase biotechnological techniques such as recombinant DNA Xylanase can be broadly classified into three types on technology, several attempts have been made to iden- the basis of (a) molecular mass and isoelectric point, tify, isolate and clone the gene encoding for xylanase in (b) crystal structure and (c) catalytic/kinetic property a suitable system. This approach helps in the engineer - (Wong et al. 1988; Jeffries 1996; Biely et al. 1997; Liu and ing of efficient microorganisms for enhanced xylanase Kokare 2017). On basis of molecular mass and isoelectric production with desired properties. This review gives point, the xylanase was classified into two groups, i.e., (a) a comprehensive insight into xylanase classification, its high-molecular weight with low isoelectric (acidic) point mode of action, different xylanase sources with available (HMWLI) and (b) low-molecular weight with high iso- production methods and its optimization strategies for electric (basic) point (LMWHI). However, several excep- enhanced production. The review also gives a brief idea tions to this classification have been observed where about different strategies employed for xylanase purifi - not all xylanases fall in the category of HMWLI (above cation and characterization, biotechnological approach 30  kDa) or LMWHI (below 30  kDa) (Collins et  al. 2002, for enhanced xylanase production with desired prop- 2005). Therefore, a more appropriate system includ - erties which are further used for different industrial ing primary structure (crystal), comparison of catalytic applications. domain with mechanistic features such as kinetic, cata- lytic property, substrate specificity, and product descrip - Structure of xylan and role of xylanolytic enzymes tion was introduced (Henrissat and Coutinho 2001; in its breakdown Collins et  al. 2005). The genomic, structural (3D crystal Xylan consists of d-xylose backbone linked with β-1,4- structure) and functional information of xylanase is avail- glycosidic bonds and l-arabinose traces forming into able under glycoside hydrolase (GH) families available on a complex heteropolymeric structure. Xylan is present carbohydrate-active enzyme (CAZy) database. in various biomasses that have several forms such as The CAZy is knowledge-based, highly curated database in hardwoods as O-acetyl-4-O-methylglucuronoxy- on enzymes that play a key role in breakdown, modifica - lan, in softwoods as arabino-4-O-methylglucuronox- tion, and assembly of glycosidic bonds in carbohydrates ylan and in grasses and annual plants as arabinoxylans. and glycoconjugates. It consists of genomic, sequence These residues can be substituted with acetyl, feruloyl, annotation, family classifications, structural (3D crystal) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 3 of 36 Fig. 1 Structure of xylan showing bonds which are attacked by specific xylanolytic enzyme for complete hydrolysis of xylan to its constituents (Adapted from Beg et al. 2001, Lange 2017) and functional (biochemical) information on carbohy- inversion (Subramaniyan and Prema 2002; Lombard et al. drate-active enzyme from publicly available resources 2014). such as National Center for Biotechnology Information, NCBI (Lombard et al. 2014). Retention The major GH families associated with xylanase are This process is represented by double displacement 5, 7, 8, 9, 10, 11, 12, 16, 26, 30, 43, 44, 51, and 62. The mechanism with α-glycosyl and oxo-carbonium inter- GH families 5, 7, 8, 10, 11, and 43 have a single distinct mediate formation followed by its subsequent hydrolysis. catalytic domain, whereas enzymes grouped under GH Glutamate residues play a vital role in the catalytic mech- families 16, 51, and 62 have two catalytic domains with anism. First, two carboxylic acid residues present in the bi-functional property (Collins et  al. 2005). The enzyme active site result in α-glycosyl enzyme intermediate for- grouped under GH families 9, 12, 26, 30, and 44 has mation. The intermediate formation occurs via protona - secondary xylanase activity. Based on the hydrophobic tion of the substrate by a carboxylic acid residue acting cluster analysis of the catalytic domains along with simi- as an acid catalyst and departure of the leaving group due larities studies of amino acid sequences, xylanases have to nucleophilic attack caused by another carboxylic acid. been primarily classified as GH 10 and GH 11 (Verma This collectively results in β to α inversion due to the and Satyanarayana 2012a). The catalytic properties of α-glycosyl enzyme intermediate formation. Second, the GH 10 and GH 11 have been studied extensively, whereas first carboxylate group abstracts a proton from a nucleo - the information on GH families 5, 7, 8 and 43 is very philic water molecule and attacks the anomeric carbon limited (Taibi et  al. 2012). Different structural and func - resulting in second substitution, where the anomeric tional properties of different GH families are tabulated in carbon gives rise to product with the β configuration (α Table 1. to β inversion) via a transition state of oxo-carbonium ions (Fig.  2) (Collins et  al. 2005; Lombard et  al. 2014). Mode of action of xylanases grouped under various GH Enzymes of families 5, 7, 10, and 11 mostly work on the families principle of retention. There is the difference in structure, physicochemical properties, substrate specificities and mode of action Inversion of members of GH families 5, 7, 8, 10, 11 and 43 (Col- The enzymes of families 8 and 43 act via inversion of lins et al. 2005). The hydrolysis of xylan by xylanase may the anomeric center with glutamate and aspartate as occur by two different mechanisms, i.e., retention or the major catalytic residue. This is a single displacement mechanism, in which only one carboxylate ion offers Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 4 of 36 Table 1 Classification of glycoside hydrolases (GH) family consisting of xylanase GH family Clan Activities in family Properties Mode of action References Structure Functional GH 5 GH-A endo-β-1,4-Xylanase; Consist of seven amino acid Largest GH family CNB-Glu Collins et al. (2005), Lombard et al. β-glucosidase cellulase (β/α) barrel fold Substitute on main xylan chain CPD-Glu (2014) Highly conserved Retaining GH 7 GH-B endo-β-1,4-Glucanase High-molecular weight and low pI Common characteristics with fam- CNB-Glu Collins et al. (2005), Lombard et al. β-Jelly roll ily 10 and 11 CPD-Glu (2014) small substrate-binding site (4 Retaining subsite and 1 catalytic site) GH 8 GH-M Cellulases; chitosanases; (α/α) fold Cold-adapted CNB-Asp Collins et al. (2002, 2005), Lombard lichenases; endo-1,4-β-xylanases Large substrate-binding cleft Break xylan into X3 and X4 CPD-Glu et al. (2014) Highly active on long-chain XOS Inversion of the anomeric GH 10 Family G GH-A endo-1,4-β-Xylanases; endo-1,3-β- Low-molecular mass high pI Attack on aryl β-glycosides and CNB-Glu Ahmed et al. (2009), Collins et al. xylanases (8–9.5) aglyconic bond of X2 and X3, CPD-Glu (2005), Lombard et al. (2014), (α/β) barrel fold respectively Retaining Motta et al. (2013) Small yet numerous (4–5) Highly active on short XOS substrate-binding sites GH11 GH-C xylanases “true xylanases” (active High MW and lower pI values Attack on aryl β-glycosides and CNB-Glu Ahmed et al. (2009), Collins et al. on xylose substrate) β-Jelly roll aglyconic bond of X2 and X3, CPD-Glu (2005), Lombard et al. (2014), Small size respectively Retaining Motta et al. (2013) Large substrate-binding clefts (7 Inactive on aryl cellobiosides subsites) High substrate selectivity and catalytic efficiency Wide pH and temperature stability Cold-adapted Highly active on long-chain XOS GH 43 GH-F β-Xylosidase β-Propeller (5 blade) fold Debranching and degradation of CNB-Asp Collins et al. (2005), Lombard et al. α-l -Arabinofuranosidase; xylanase Catalytic residue glutamate and hemicellulose polymer CPD-Glu (2014), Mewis et al. (2016) aspartate in the center Inverting single displace- ment mechanism X2, xylobiose; X3, xylotriose; X4, xylotetraose; XOS, xylooligosaccharides; CNB, catalytic nucleophile/base; CPD, catalytic proton donor; Asp, aspartic acid; Glu, glutamic acid Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 5 of 36 licheniformis DMS xylanase had both the properties of endoxylanase and appendage dependent xylanase activ- ity. It showed equal production of both xylobiose and xylotriose by hydrolysis of the commercial substrate and agro-waste such as corn cob (Ghosh et al. 2019). Thermothelomyces thermophila (TtXyn30A) that hydrolyzes xylan into xylose and two acidic xylooligosac- charides, namely xylotriose (M eGlcA Xyl3) and xylobi- ose, i.e., MeGlcA Xyl , was studied. TtXyn30A catalyzed the release of the disaccharide xylobiose from the non- reducing end of xylooligosaccharides, thus exhibiting an exo-acting catalytic behavior. TtXyn30A also showed the capability to cleave linear parts of xylan and uronic xylo- oligosaccharides as well as resulting in the formation of aldotriuronic and aldotetrauronic acid (Katsimpouras Fig. 2 Mode of action of xylanase: retention et al. 2019). Puchart et al. (2018) have reported the mode of action of hydrolysis of eucalyptus plant using endoxy- lanase belonging to GH10, GH11, and GH30 family. All the endoxylanse resulted in the formation of acetylated XOS. The GH10 endoxylanase results in short xylo - oligosaccharides, whereas GH30 endoxylanase results in longer xylooligosaccharides. An acetyl esterase (AcXEs) played a key role in understanding the plant decay or depolymerization mechanism and also showed efficiency in plant biomass bioconversion (Rytioja et al. 2014). A novel modular endoxylanase with transglycosyla- tion activity was reported from Cellulosimicrobium sp. HY-13 belonging to GH6 family (Ham et  al. 2012). A GH30 family xylanase XynA was reported from Erwinia chrysanthemi belonging to subfamily 8 with the special property of hydrolyzing 4-O-methyl-glucuronoxylan (Urbániková et  al. 2011). Xyn11B from thermophilic Fig. 3 Mode of action of xylanase: inversion fungus Humicola insolens Y1 encoding multi-cellular xylanase belonged to GH11 reported by Shi et al. (2015). Bacteroides intestinalis DSM17393, a xylan degrading for overall acid catalyzed group departure (Fig.  3). This human gut bacterium, reported the presence of two puta- enzyme also acts as the base for activating a nucleophilic tive GH8 xylanases which hydrolyze both xylopentose water molecule to attack the anomeric carbon (depend- and xylohexose (Hong et  al. 2014). Endoxylanase XynB ing on the distance between two molecules) for breaking from marine bacterium Glaciecola mesophila KMM241 the glycosidic bonds and causing inversion of anomeric with xylan binding ability and GH8 catalytic domain was carbon configuration (Collins et  al. 2005; Motta et  al. reported by Guo et al. (2013). 2013; Lombard et al. 2014). Several attempts have been made to understand the Mechanism for glycosidic hydrolase family 10 mode of action of xylanase obtained for different organ - (GH10) isms. An unusual mode of action of GH8 xylanase Among all the above-mentioned GH families, GH 10 (β-xylosidase, an α-arabinofuranosidase, and an acety- consists of endoxylanase, e.g., endo-1,4-β-xylanases, lesterase activity) was observed in Pseudoalteromonas endo-1,3-β-xylanases and cellobiohydrolases (Collins atlantica, which showed the presence of a long tail of et  al. 2005). Endo-1,4-β-xylanases or xylanase mainly unsubstituted xylose residue on the reducing end of oli- comes under this GH10 family. It usually consists of gosaccharides produced (Ray et  al. 2019). Thermophilic high-molecular weight xylanase with low isoelectric xylanase obtained from Bacillus licheniformis DMS has points and displays an (α/β) -barrel fold. This structure novel hydrolysis properties similar to GH30. It breaks mimics the shape of a ‘Salad Bowl’, because of an enlarged the linear β-(1-4) linkage of beech wood and birchwood loop architecture, one face of the molecule is having xylan along with glucuronoxylan and arabinoxylan. B. Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 6 of 36 ~ 45 Å large radius and the other face is having ~ 30 Å 2006). Hu et  al. (2011) proposed a model holocellulosic radius because of simple (α/β) turns (Zhang et al. 2016a, substrate, i.e., mixture of pure cellulose and 10% pre- 2016b). However, these two categories are relatively the deacetylated commercial birchwood xylan to understand same because along with sharing similar fold also shares the synergism between two family xylanase and cellulase some common residues and has similar catalytic mecha- (during the xylan extraction process). This study showed nisms. The xylanase belonging to GH 10 family has low that substrate deacetylation has increased the hydrolytic substrate specificity and, however, exhibits high catalytic performance of GH11 as the acetyl group restricted the versatility than that of GH 11 family. Xylanase belonging accessibility of xylan more for GH11 than GH10. Ther - to GH10 family exhibits greater catalytic versatility and mostability is the second factor for better performance of lower substrate specificity as compared to those belong - GH10 endoxylanase over GH11 because lignocellulosic ing to GH11 (Biely et  al. 1997; Faulds et  al. 2006; Motta biomass hydrolysis occurs better at high temperature et  al. 2013). GH10 xylanase attacks the xylose linkages (50 °C) and 2–3 days long-time duration. which are closer to the side-chain residues (Dodd and Cann 2009). This could be explained by fact that the Source for xylanase production xylose residues bind at subsites (Fig.  4) on xylanase that The xylanase is ubiquitous in nature and its presence is causes cleavage of the bond between the monomeric observed diversely in a wide range of living organisms, residues at the non-reducing (− 1) and the reducing end such as marine, terrestrial and rumen bacteria (Chakdar (+ 1) of the polysaccharide substrate (Davies et al. 1997). et  al. 2016), thermophilic and mesophilic fungi (Chadha Maslen et al. (2007) demonstrated that when arabinox- et  al. 2019; Singh et  al. 2019), protozoa (Devillard et  al. ylan was hydrolyzed by GH10 and GH11 xylanase, the 1999; Béra-Maillet et  al. 2005), crustaceans (Izumi et  al. products generated have arabinose residues substituted 1997), snails (Suzuki et  al. 1991), insects (Brennan et  al. on xylose at the + 1 subsite and + 2 subsites, respectively. 2004), algae (Jensen et al. 2018), plants and seeds (imma- Therefore, xylanases from family 11 and 10 preferentially ture cucumber seeds and germinating barley) (Bae et  al. cleave the unsubstituted regions of the arabinoxylan 2008; Sizova et  al. 2011). Bacteria and fungus are widely backbone and the unhampered substituted regions along used for industrial production of xylanase. Several micro- the xylan backbone (Biely et al. 1997; Motta et al. 2013). bial sources of xylanase are classified in Table 2. The degree of side-chain decorations of xylan influences the specificity of the enzyme toward substrates and, thus, Bacterial sources of xylanase has an important implication on the hydrolytic prod- Among bacteria, Bacillus species have been reported uct formation by xylan deconstruction (Dodd and Cann widely as the most potent xylanolytic enzyme producers 2009). Yang and Han (2018) demonstrated the positional such as Bacillus sp., B. halodurans (Gupta et  al. 2015), binding and substrate interaction of GH10 xylanase of B. pumilus (Thomas et  al. 2014), B. subtilis (Banka et  al. Thermotoga maritime using molecular docking approach. 2014), B. amyloliquefaciens, B. circulans, and B. stearo- Researchers have reported in their previous studies thermophilus (Chakdar et  al. 2016). Xylanase with high that GH10 endoxylanase had better performance than temperature stability, acid/alkali stability, and cold adapt- GH11 in synergy with cellulase enzyme for pretreated lig- ability have been isolated and purified from a wide range nocellulosic biomass hydrolysis. The reason behind this of bacteria found in extreme environment. Thermo - may be because GH11 endoxylanase has the lower acces- tolerant xylanase active at a very high temperature of sibility toward acetylated xylan backbone (Faulds et  al. 60–70 °C has been reported from Bacillus spp. (Thomas Fig. 4 Schematic representation of site for attack of GH10 xylanase on xylan Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 7 of 36 Table 2 Microbial sources of xylanase Xylanase producing microorganisms Major group Genus Species References Bacteria Arthrobacter Arthrobacter sp. Murugan et al. (2011) Geobacillus Geobacillus thermoleovorans, Geobacillus stearothermophilus Gerasimova and Kuisiene (2012), Verma and Satyanarayana (2012a, b), Bibi et al. Geobacillus thermodenitrificans (2014) Pediococcus Pediococcus acidilactici Adiguzel et al. (2019) Bacillus Bacillus firmus, Bacillus arseniciselenatis, Bacillus licheniformis, Bacillus amylolique - John et al. (2006), Bajaj and Manhas (2012), Kamble and Jadhav (2012), Amore faciens, Bacillus subtilis et al.(2015) Clostridium Clostridium thermocellum, Clostridium papyrosolvens Pohlschroder et al. (1994), Heinze et al. (2017) Dictyoglomus Dictyoglomus thermophilum Zhang et al. (2010b) Paenibacillus Paenibacillus sp., Paenibacillus xylanilyticus, Paenibacillus terrae, Paenibacillus Shi et al. (2010), Valenzuela et al. (2010), Sharma et al. (2013), Song et al. (2014) barcinonensis, Paenibacillus macquariensis Rhodothermus Rhodothermus marinus Abou Hachem et al. (2000) Staphylococcus Staphylococcus aureus, Staphylococcus sp. Gupta et al. (2000), Iloduba et al. (2016) Pseudomonas Pseudomonas sp., Pseudomonas aeruginosa, Pseudomonas fluorescens subsp. Raghothama et al. (2000), Xu et al. (2005), Iloduba et al. (2016), Lin et al. (2017), cellulose, Pseudomonas boreopolis, Pseudomonas stutzeri Purkan et al. (2017), Lee et al. (2018) Thermoactinomyces Thermoactinomyces thalophilus, Thermoactinomyces vulgaris Kohli et al. (2001), Selim (2016) Thermotoga Thermotoga maritima Velikodvorskaya et al. (1997), Shi et al. (2013), Yoon et al. (2014) Thermotoga thermarum Thermotoga neapolitana Actinomycetes Streptomyces Streptomyces sp., Streptomyces lividans Shibuya et al. (2000), Verma and Satyanarayana (2012a, b) Kitasatospora Kitasatospora sp. Rahmani et al. (2018) Nonomuraea Nonomuraea flexuosa, Nonomuraea jabiensis sp. Paloheimo et al. (2007), Camas et al. (2013) Actinomadura Actinomadura geliboluensis, Actinomadura sp. Verma and Satyanarayana (2012a, b), Adigüzel and Tunçer (2017) Cellulomonas Cellulomonas fimi, Cellulomonas flavigena, Cellulomonas uda Notenboom et al. (1998), Murugan and Jampala (2015), Lisov et al. (2017) Microbacterium Microbacterium xylanilyticum sp., Microbacterium soli sp. Kim et al. (2005), Srinivasan et al. (2010) Micrococcus Micrococcus luteus, Micrococcus sp. Gessesse and Mamo (1998), Mmango-Kaseke et al. (2016) Thermomonospora Thermomonospora fusca, Thermomonospora curvata Irwin et al. (1994), Stutzenberger (1994) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 8 of 36 Table 2 (continued) Xylanase producing microorganisms Major group Genus Species References Fungus Talaromyces Talaromyces byssochlamydoides, Talaromyces emersonii Yoshioka et al. (1981), Waters et al. (2011) Thermomyces Thermomyces lanuginosus Alam et al. (1994) Thermoascus Thermoascus aurantiacus, Thermoascus aurantiacus var. levisporus Vardakou et al. (2005), Chanwicha et al. (2015) Melanocarpus Melanocarpus albomyces Gupta et al. (2013) Chaetomium Chaetomium thermophilum, Chaetomium globosum Gandhi et al. (1994), Latif et al. (2006) Fusarium Fusarium sp., Fusarium solani, Fusarium proliferatum, Fusarium oxysporum, Saha (2002), Imad et al. (2011), Paulo et al. (2014), Adesina et al. (2017), Gascoigne Fusarium heterosporum, Fusarium roseum and Gascoigne (2019) Humicola Humicola sp. Humicola insolens, Humicola lanuginosa, Humicola grisea da Silva et al. (1994), Monti et al. (2003), Kamra and Satyanarayana (2004), Shi et al. (2015) Paecylomyces Paecylomyces variotii, Paecilomyces themophila Krishnamurthy and Vithayathil (1989), Zhang et al. (2010a) Scytalidium Scytalidium thermophilum, Scytalidium acidophilum Joshi and Khare (2012) Al Balaa et al. (2006) Thielavia Thielavia sp., Thielavia terrestaris Garcia-Huante et al. (2017), Thanh et al. (2019) Berka et al. (2011) Corynascus Corynascus sepedonium Sharma et al. (2008) Myceliophthora Myceliophthora heterothallica, Myceliophthora fergusii van den Brink et al. (2013) Sporotrichum Sporotrichum thermophile El-Naghy et al. (1991), Sadaf and Khare (2014), Topakas et al. (2003) Rhizomucor Rhizomucor pusillus Hüttner et al. (2018) Trichoderma Trichoderma inhamatum, Trichoderma piluliferum, Trichoderma viride, Tricho- Azin et al. (2007), da Silva et al. (2015), Carvalho et al. (2017), Tang et al. (2017), derma longibrachiatum, Trichoderma asperellum, Trichoderma stromaticum, Syuan et al. (2018), da Costa et al. (2019), Ezeilo et al. (2019) Trichoderma harzianum, Trichoderma reesei Aspergillus Aspergillus niger, Aspergillus flavus, Aspergillus niveus, Aspergillus ochraceus, Asper - Gawande and Kamat (1999), Betini et al. (2009), Ang et al. (2013), Dhulappa and gillus foetidus, Aspergillus fumigates, Aspergillus terreus, Aspergillus tamari Lingappa (2013), de Guimaraes et al. (2013), De Queiroz Brito Cunha et al. 2018a, b Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 9 of 36 et  al. 2014), Bacillus Halodurans TSEV1 (Kumar and understanding of the physiology and different metabolic Satyanarayana 2014), Clostridium thermocellum (Fer- processes of the microbial system has led to an improve- nandes et  al. 2015), Rhodothermus marinus (Karlsson ment in the fermentation process. However, there is still et  al. 2004), Streptomyces sp. (Sukhumsirichart et  al. an opportunity to improve the yield of enzymes. The 2014), Stenotrophomonas maltophila (Raj et  al. 2013), optimization of the xylanase production will be discussed Thermotoga thermarum (Shi et  al. 2013). Psychrophilic in a later section. xylanases are not very common but found to be isolated The xylanase production has been carried out under from several bacteria such as Clostridium sp. PXLY1 submerged fermentation (SmF) and solid-state fer- (Akila and Chandra 2003), Flavobacterium sp. MSY-2 mentation (SSF) (Motta et  al. 2013). The choice of the and Flavobacterium frigidarium (Humphry et  al. 2001; fermentation process usually depends on the type of Dornez et  al. 2011) Pseudoalteromonas haloplanktis microorganisms used (Table  3). Bacteria require a high TAH3A (Van Petegem et al. 2002). amount of water during growth; therefore, SmF is pre- Several alkali stable xylanases have been isolated from ferred whereas fungi due to its mycelia nature require firmicutes such as B. pumilus (Thomas et  al. 2014), B. less moisture and can be grown under SSF (Walia et  al. halodurans TSEV1 (Kumar and Satyanarayana 2014) and 2017). Several reports suggest that submerged fermen- Geobacillus thermoleovorans (Verma and Satyanarayana tation using bacteria and fungi is the most preferred 2012b) and actinomycetes such as Actinomadura sp. method for xylanase production. Statistically speaking Cpt20 (Taibi et  al. 2012) and Streptomyces althioticus approximately 90% of total xylanase is produced globally LMZM (Luo et al. 2016). through SmF. During SmF, the synergistic effect of differ - ent xylan degrading enzymes can be observed and even result in better biomass utilization for enhanced xyla- Fungal sources of xylanases nase production (Polizeli et  al. 2005; Bajpai 2014). Xyla- The mesophilic fungi of genera Aspergillus and Tricho- nase production utilizes soybean residues and rice straw derma are well known to be potent xylanase producer as a substrate under SmF by Aspergillus oryzae LC1 and and most widely used for commercial production. iel Th a - Aspergillus foetidus (Bhardwaj et  al. 2017; De Queiroz via terrestris, (Garcia-Huante et  al. 2017), Talaromyces Brito Cunha et al. 2018a, b). Similarly, Irfan et al. (2016) thermophilus (Maalej et  al. 2009), Paecilomyces thermo- suggested the production of xylanase under SmF by B. phile (Fan et  al. 2012), Achaetomium sp. X2-8 (Chadha subtilis BS04 and B. megaterium BM07. Different advan - et  al. 2019), Rhizomucor pusillus (Hüttner et  al. 2018), tages of the SmF are homogenous condition throughout Rasamsonia emersonii, (Martínez et al. 2016) T. Leycetta- medium; method is well characterized and can be easily nus (Wang et al. 2017), Melanocarpus albomyces (Gupta scaled up (Guleria et al. 2013). There are some disadvan - et  al. 2013) and Aspergillus oryzae LC1 (Bhardwaj et  al. tages to SmF as well which limit its industrial application, 2019) were found to be producer of hyper-thermophilic i.e., high maintenance cost, energy intensive and complex active xylanase. Several alkali stable xylanases were downstream (Virupakshi et al. 2005; Walia et al. 2017). obtained from different fungal strains such as Paeniba - Recent trends suggest that xylanase production by SSF cillus barcinonensis (Valenzuela et  al. 2010), Aspergillus is also gaining popularity (Walia et  al. 2014). Bacillus fumigatus MA28 (Bajaj and Abbass 2011), Cladosporium sp. was used for the production of thermo-alkalophillic oxysporum (Guan et al. 2016) and Aspergillus oryzae LC1 extracellular xylanase under SSF using wheat bran as (Bhardwaj et al. 2019). substrate (Kamble and Jadhav  2012). Similarly, SSF of Trichoderma koeningi using corn cob supplemented with pineapple peel powder showed enhanced production Strategies employed for xylanase production of xylanase (Bandikari et  al. 2014).  It has several advan- from different microbial sources tages such as low cultivation, operation and capital cost, The production of xylanase from microorganisms is a lower rate of contamination, easy enzyme recovery, and affected by the fermentation process employed, choice of high productivity per reactor volume. The disadvantages substrate and different media components. These com - associated with SSF are not suitable for all microorgan- ponents are often regulated by different process opti - isms (preferred for the fungal system) and require proper mization for enhanced production of the enzyme for its aeration and humidity control and up-scaling is a tedious application at large scale. process (Mienda et al. 2011). Different fermentation process employed for xylanase Selection of suitable substrate for xylanase production production: submerged and solid‑state fermentation Quantity and quality of the fermentation product vary Xylanases are produced by a different fermentation with different substrates. There are various commercially process using various microorganisms. The better Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 10 of 36 Table 3 Production system, characteristic properties and application of xylanase from different microorganisms Microbes Substrate Fermentation MW (kDa) Optimum Stability Metal activator Application References Temperature (°C) pH Temperature (°C) pH Bacteria Bacillus altitudedi- Sorghum straw SmF 98 50 8 35–70 3–10 Ca, Mn, K, Na, Fe Deinking of waste Adhyaru et al. (2017) nus hand-written paper pulp Paenibacillus baren- Birch wood xylan, SmF 116 60 6.5 20–65 4–11 Mg, Ca, Ba, Co XOS production Liu et al. (2018) goltzii beechwood xylan, oat-spelt xylan Burkholderia sp. Wheat Bran SmF – 50 8.6 30–50 6–9 Co, Na, Ba, Mg, K Hydrolysis of ligno- Mohana et al. (2008) DMAX cellulosic biomass Bacillus licheni- Wheat Bran SmF 46 60 9 30–100 4–11 Fe, Mn Kraft pulp bio- Raj et al. (2018) formis Mg, Zn bleaching Ca, Ni Anoxybacillus Beech wood xylan SmF 37 65 9 30–65 6–9 – Thermo-alkaline Yadav et al. (2018) kamchatkensis stable xylanase NASTPD13 suitable for indus- trial application Pediococcus acidi- Oatmeal SmF 48.15 40 7 20–50 2–9 K, Ba, Cd, Co, Sr, Mg, Clarification of fruit Adiguzel et al. (2019) lactici GC25 Ca, Al, Zn, Ni juice Pseudomonas Wheat Bran SmF 20 65 6 55–75 5–9 – Thermo-alkali stable Lin et al. (2017) boreopolis LUQ1 xylanase for indus- trial application Geobacillus sp. Corncob, beech- SmF 45 75 7 50–85 5–9 Cu, Zn, K, Fe, Ca, Zn, Ethanol Generation Bibra et al. (2018) Strain DUSELR13 wood Mg, Na Actinomycetes Streptomyces oliva- Birch wood Xylan SmF 23 40 7 20–70 5–11 Na, Cu, Co, Fe, Zn, Pretreated biomass Sanjivkumar et al. ceus (MSU3) Mg, Mn hydrolysis for (2017) bioethanol pro- duction Streptomyces Beech wood xylan SmF 46.2 65 6.5 50–70 4–11.5 Ca, Co, Mn XOS production Boonchuay et al. thermovulgaris (2016) TISTR1948 Kitasatospora sp Sugarcane bagasse SmF 49.3 50 5 30–80 4–7 Zn, EDTA XOS production Rahmani et al. (2019) Actinomadura sp. 20.11 80 10 60–90 5–10 Mn, Ca, Cu Paper and Pulp Taibi et al. (2012) strain Cpt20 Industry Fungus Trichoderma Rice straw SSF – 60 5 30–60 3–10 – Textile processing El et al. (2018) longibrachiatum efficient desizing KT693225 and bioscouring, Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 11 of 36 Table 3 (continued) Microbes Substrate Fermentation MW (kDa) Optimum Stability Metal activator Application References Temperature (°C) pH Temperature (°C) pH Trichoderma viride Rice bran, sugarcane SSF 14 50 7 25–50 3–9 Zn, Fe, Mg, Mn, Ca Bio-bleaching of Nathan et al. (2017) VKF3 bagasse, coconut newspaper oil cake, ground- nut oil cake, neem oil cake Trichoderma pilu- Wheat bran SSF – 50 4.5 30–60 3–10 – Additives for bovine da Costa et al. (2019) liferum feeding Humicola insolens wheat bran SmF 44 70–80 6–7 40–80 5–10 Brewing Industries Du et al. (2013) Y1 and XOS genera- tion Pichia stipitis corn cob wheat bran SSF 31.6 50 6 40–60 3.0–11.0 Cu, K XOS generation Ding et al. (2018) Fusarium sp Wood shaving SSF – – – 25–55 4–9 – Paper and pulp Adesina et al. (2017) bleaching Thermomyces wheat bran SmF – 47.9 7.3 30–65 3.0–10.0 Mg, Na, K Fermentable sugar Kumar and Shukla lanuginosus production, pulp (2018) bleaching Thermoascus Wheat Bran SmF 31 75 5 30–80 2–10 Mn, Ag – Ping et al. (2018) aurantiacus Schizophyllum com- Rice straw SSF – 55 5 30–65 4–7 Na, K, Ca Kraft pre-bleaching Gautam et al. (2018) mune ARC-11 Aspergillus oryzae Rice straw SmF 35 25 5 25–60 3–10 Fe, Ag, Mg, Mn, Co Hydrolysis of Agro- Bhardwaj et al. (2017, LC1 residues and XOS 2019) Production SmF, submerged fermentation; SSF, solid-state fermentation; XOS, xylooligosaccahrides Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 12 of 36 available substrates, i.e., xylan, carboxymethyl cellulose the type and level of nitrogen source in the media is an (CMC), pectin, and starch for, i.e., xylanase, cellulase, important parameter (Seyis and Aksoz 2005; Naveen pectinase, and amylase, respectively (Barman et al. 2015; et  al. 2014; Irfan et  al. 2016). Trace elements, amino Bhardwaj et al. 2017; Kumar et al. 2018a). Due to the high acids, and vitamins are also important parameters for the cost of commercial substrates and considering the eco- growth of different microorganisms (Simair et  al. 2010; nomic feasibility of the process, scientists are working Bibra et al. 2018). Therefore, regulating their levels in the from past several years to find alternative substrates for media is important for regulating the production of xyla- the production of these enzymes. nase. Also, the addition of biosurfactant such as Tween Agrowastes and other organic wastes (domestic and 80 affected the level of xylanase production (Liu et  al. industrial) are used as a carbon source for the production 2006; Kumar et al. 2013). of xylanase with the focus on sustainability and best uti- lization of these wastes (Table 3). Some of the most com- Strategies employed for the selection monly used agro-residues for xylanase production are of the method of xylanase production and its wheat bran, wheat husk (Kumar et al. 2018a, b, c, d), rice optimization straw (Bhardwaj et al. 2017), rice husk, sugarcane bagasse Intially a  common minimal media providing essential (Suleman and Aujla 2016), coconut coir, coconut oil cake nutrients to the growth of microorganisms are used. (Rosmine et  al. 2019), groundnut shell (Namasivayam This  will allow to  check the strains are capable of pro - et  al. 2015), wood pulp (Kalpana and Rajeswari 2015), ducing required enzymes/metabolite of desired interest. sawdust, chilli post-harvest (Sindhu et  al. 2017), corn- Then, the process is further optimized for higher produc - cobs, molasses, sugar beet pulp fruit, and vegetable waste tion of enzymes from the strain (Walia et  al. 2017). For (Bandikari et  al. 2014). Recent studies also showed that the production of desired product, different strategies are wastewater from pulp industry was reused as media for used for improving yield such as optimization of media xylanase production (de Queiroz-Fernandes et al. 2017). components, regulating physical growth parameters, and improving the strain by use of the different biotechno - Role of important media components used for xylanase logical tool (Sharma 2017). The schematic representation production of the methodology adapted for production, purification Naturally, xylanolytic enzymes are induced by the differ - and characterization of xylanase are shown in Fig.  5.  In ent intermediate products generated by their own action. this section, the focus will be on the optimization of Xylan is found to be best xylanase inducer (Taibi et  al. media and growth parameters and biotechnological 2012; Guleria et  al. 2013; Walia et  al. 2013, 2014). How- tool approach will be discussed in a later section. Dur- ever, xylan being a high-molecular weight polymer can- ing SmF for enzyme production, different components not stimulate xylanase as it cannot enter the microbial which need to be optimized are selection of substrate and cells. Therefore, a small amount of constitutive enzyme microorganisms, regulation of nutrients concentration produced in the media results in the generation of low- in media, i.e., carbon, nitrogen, trace elements, vitamins molecular weight fragments, i.e., xylobiose, xylotriose, and amino acids, and physical parameters, i.e., tempera- xylotetraose, xylose from the breakdown of xylan and ture, pH, agitation, aeration, inoculum sizes, and incuba- further induces the xylanolytic enzymes for enhanced tion period (Motta et al. 2013; Walia et al. 2015a, 2017). enzyme production (Walia et  al. 2017). Cellulose, syn- During optimization of the SSF, there is requirement thetic alkyl, aryl β-d xylosides, and methyl β-d-xyloside of regulating particle size, pretreatment, humidity, water also act as an inducer for xylanolytic enzyme production content and water activity (a ) of substrate, type and size (Thomas et  al. 2013). Busk and Lange (2013) observed of the inoculums, removal of extra heat generated during that poor quality paper can efficiently induce the xyla - microbial metabolism and most importantly maintaining nase production in Thermoascus aurantiacus even in the the uniform environment (temperature) and evolution of absence of xylan and xylooligosaccharides. CO and consumption of O , i.e., gaseous system (Muru- 2 2 Nitrogen is an important structural element required gan et al. 2011; Behera and Ray 2016; Behnam et al. 2016; for the metabolic processes in the microbial system. Leite et al. 2016; Walia et al. 2017). Therefore, the choice of nitrogen source is important for the growth of microorganisms that subsequently affect Approach for enhanced xylanase production: one factor the overall enzyme yield. Peptone, tryptone, soymeal, at a time (OFAT) yeast extract, etc. have found to be suitable nitrogen To proceed for the optimization of the xylanase produc- source. The requirement of these nitrogen sources var - tion, one factor at a time (OFAT) approach is used for ies for different microorganisms; therefore, optimizing the selection of important factors affecting the xylanase Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 13 of 36 Fig. 5 Schematic representation of the methodology for production, purification and characterization of xylanase yield. In the OFAT approach, one factor is kept variable parameters (substrate concentration) were optimized keeping other factors at constant (Bhardwaj et  al. 2018). using OFAT approach for enhanced production of xyla- The factor may be important physical or nutritional nase by T. viride-IR05 under SSF (Irfan et al. 2014). parameters regulating the growth of microorganisms and its enzyme yield. Ramanjaneyulu et  al. (2017) have Statistical approach for enhanced xylanase production evaluated several operating parameters for nutritional The OFAT approach is tedious and requires a large set of (different substrates and their concentrations, additional experiments for optimization. The recent trend suggested carbon and nitrogen sources) and physical factors (incu- the application of the statistical approach to design bation temperature, pH, agitation) along with inoculum experiments considering different factors as variable size of Fusarium  sp. BVKT R2 in a shake flask culture and performing the interaction studies among several (SmF) by OFAT approach. The high xylanase yield of physical and nutritional parameters. The statistical-based 4200 U/mL was obtained with birch wood xylan in min- approach has shown satisfactory results for optimization eral salt medium with 1.5% sorbitol (additional carbon of xylanase production using fungal and bacterial strains source), 1.5% yeast extract (nitrogen source) at tempera- with the minimum number of experimental sets (Gule- ture of 30 °C, pH of 5.0, agitation of 200 rpm and inocu- ria et  al. 2015, 2016a; Walia et  al. 2015b; Bhardwaj et  al. lum of agar plugs (6) for only 5  days incubation. Under 2017). unoptimized condition, xylanase yield was only 1290 U/ Response surface methodology (RSM) was employed mL after 7 days of incubation, thus improving by 3.2-fold. to optimize the fermentation medium constituents and Bhardwaj et  al. (2018) also optimized xylanase produc- the physical factors affecting xylanase production using tion using Aspergillus oryzae LC1 using OFAT approach. Bacillus tequilensis strain ARMATI under SmF (Khusro The physical parameters (liquid to solid ratio, pH, inocu - et  al. 2016). The experimental design consists of cen - lums size, incubation time and temperature) and nutrient tral composite design (CCD) with four (4) independent Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 14 of 36 variable (carbon and nitrogen source, temperature and biotechnological approaches are used for improving time) resulting in 30 experimental runs. The central com - the yield and imparting characteristic properties to posite design gave an optimum parameter for studied the desired enzyme. These approaches involve genetic variable (1.5% w/v birchwood xylan, 1% w/v yeast extract, manipulation involving mutation and recombinant DNA temperature 40 °C, time 24 h) showing 3.7-fold enhanced technology. xylanase production as compared to OFAT. High coef- ficient of determination (R ) of 0.9978 with p < 0.05 as Mutagenesis of microorganisms for enhanced xylanase obtained by analysis of variance (ANOVA) analysis sug- production gested the accuracy of the overall process at a significant Several researchers suggested that the application of level. The R value of 0.9978 represents that sample varia- physical mutagens such as UV radiation (Rahim et  al. tion of 99.78% and only 0.21% of the total variation in the 2009; Abdel-Aziz et  al. 2011) and chemical mutagens response cannot be explained by the model. The xylanase such as N-methyl N-nitro N-nitroso guanidine (MNNG) obtained has shown high thermal (60  °C) and alkali sta- (Haq et  al. 2004, 2008) resulted in enhanced xylanase bility (pH 9). Bhardwaj et al. (2017) optimized nutritional production. Burlacu et  al. (2017) demonstrated the components (rice straw, MgSO , and CaCl concentra- 4 2 improvement of xylanase production in fungal strains, tion) and physical parameters (temperature and pH) for i.e., Aspergillus brasiliensis and Penicillium digitatum by enhanced xylanase production with an Aspergillus oryzae physical mutagenesis (5–50  min, exposure to UV light) LC1 under submerged fermentation using CCD-RSM. and chemical mutagenesis (150  µg/mL of N-methyl-N′- The statistical design suggested optimum condition of nitro-N-nitrosoguanidine or ethyl methane sulfonate). 1% rice straw (w/v), 1.0  g/L C aCl , and 0.3  g/L M gSO , 2 4 The exposure to physical and chemical mutagens has with pH 5 and 25  °C. It resulted in maximum xylanase resulted in significant changes in the mutant strain as activity of 935 ± 2.3 IU/mL which is 3.8-fold higher than compared to the wild type. Han et  al. (2017) demon- the un-optimized Mendel’s Stenberg Basal Salt medium strated the site-directed mutagenesis of XynCDBFV (245 ± 1.9  IU/mL). The enzyme showed thermal (25– gene of ruminal fungus  Neocallimastix patriciarum for 60 °C) and pH (3–10) stability. The xylanase also showed improving the thermostability of XynCDBFV, a glyco- potential for efficient enzymatic hydrolysis of different side hydrolase (GH) family 11 xylanase. Similar work lignocellulosic agro-residues. has also been carried out in different bacterial strains, a Similarly, Tai et  al. (2019) reported the optimization rifampin-resistant mutant of Cellulomonas biazotea, des- of five physical and two nutritional parameters using the ignated 7Rf, resulting in elevated levels of xylanases pro- RSM approach for enhanced xylanase production. Indig- duction as compared to the parental strain. After enous fungus Aspergillus niger DWA8 was grown under mutation, maximum xylanase and β-xylosidase pro- SSF on an oil palm frond. One physical (moisture content duction of 493  IU/L/h and 30.7  IU/L/h of β-xylosidase 75%) and one nutritional parameters (substrate concen- were obtained  respectively. This increase in xylanase tration 2.5 g) have significant effect on xylanase produc - and  β-xylosidase yield  were 1.21- and 2.29-fold higher tion. Under optimum condition,  an increase in xylanase respectively  as compared to the parental strain (Rajoka yield by  78.5% was observed as compared to an  un- et  al. 1997). Bacillus mojavensis PTCC 1723 when sub- optimized condition. The xylanase was efficiently used jected to UV light exposure (280 nm, 30 s) resulted in the for saccharification of biomass. The statistical optimiza - xylanase yield 330.6  IU/mL which is 3.45 times higher tion method for enhanced xylanase production has been as compared to 95.7  IU/mL for wild strain (Ghazi et  al. applied and widely accepted for SSF and SmF that helped 2014). Lu et al. (2016) demonstrated mutation of XynHB, in overcoming several limitations of classical empirical alkaline stable xylanase from  Bacillus pumilus  HBP8 at (OFAT) methods. N188A. The mutant XynHBN188A is expressed in E. coli and Pichia pastoris with improved xylanase yield by 1.5- Biotechnological approach for enhanced xylanase and 7.5-fold, respectively. The codon-based optimization production and high-density fermentation using Pichia pastoris sys- There is a need of high yield of the enzyme with spe - tem were utilized for improving the xylanase yield. cific properties such as high stability over a wide range of temperature and pH, high substrate specificity and Gene cloning and expression of xylanase genes using strong resistance to metal cations and chemicals for the recombinant DNA industrial application (Garg et  al. 2010;  Qiu et  al. 2010). The recombinant xylanases are designed to have equiv - The native enzyme is usually produced in low quantity alent or better properties than the wild-type enzymes and also lacks all the characteristics to meet the indus- with high yield in the expression system which can trial needs (Ahmed et  al. 2009). Therefore, different be employed in the fermentation industry. The highly Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 15 of 36 thermo-alkalophilic xylanase producing strains can be 6.5 and 85  °C, respectively. The xylanase was stable up directly employed during simultaneous saccharification to 95  °C and retained its activity in surfactants such as and fermentation for ethanol generation using lignocel- EDTA, DTT, Tween-20 and Triton X-100. lulosic biomass. The inherited stability will enable the xylanase to work efficiently even at high temperature and Expression in yeast varying pH range of the fermentation system. The heterologous protein expression in yeast system is Several reports suggests that desired xylanase gene was highly attractive due to its ability to perform eukaryotic cloned into the suitable vector followed by its expression post-translational modifications and can grow to very in the suitable microbial systems such as bacteria, yeasts, higher cell densities with the ability to secrete enzyme and fungus (Belancic et  al. 1995; Goswami et  al. 2014; into the fermentation system. Most of the yeasts are con- Jhamb and Sahoo 2012; Juturu and Wu 2012; Motta et al. sidered as GRAS organisms and do not produce toxins 2013; Nevalainen and Peterson 2014; Verma et al. 2013). (Juturu and Wu 2012). Saccharomyces cerevisiae already established as an industrial microorganism, thus, can be conveniently used for xylanase production (Ahmed et al. Expression in bacteria 2009). Goswami et  al. (2014) demonstrated the expression of a The application of Pichia pastoris as expression sys - xylanase gene from Bacillus brevis in E. coli BL21. The tem has gained impetuous because it can promote the recombinant strain predominantly secreted xylanase in expression of the protein on their own using alcohol the culture medium with 30 IU/mL xylanase activity. The oxidase as promoter using methanol utilization pathway culture filtrate is free from cellulase activity and found (Ahmed et  al. 2009; Juturu and Wu 2012; Motta et  al. to be active in a wide range of pH and temperature. A 2013). Pichia pastoris as expression system is preferred as thermo-alkali stable xylanase encoding gene (Mxyl) was it can grow to very high cell densities, inherit strong and retrieved from compost-soil metagenome library con- tightly regulated promoters, and produce high titer of struct and cloned into pET28a vector expressed in E. coli recombinant protein (g/L) both intracellularly and in the BL21(DE3). The recombinant xylanase has shown half- secretory manner (Ahmad et al. 2014). Basit et al. (2018) life of 2 h and 15 min at 80 °C and 90 °C, respectively. The demonstrated the cloning of two GH11 xylanase genes, recombinant xylanase has pH and temperature optima of MYCTH_56237  and  MYCTH_49824, from thermophilic 9.0 and 90 °C, respectively (Verma et al. 2013). fungus  Myceliophthora thermophila  and its expres- Escherichia coli is preferred and most widely used sion in  Pichia pastoris. The specific activities of purified expression host due to its inexpensive growth conditions, recombinant xylanase were observed at 1533.7 U/mg and easy manipulation, simple transformation techniques 1412.5 U/mg for MYCTH_56237  and  MYCTH_49824, requirement, high level of product accumulation in the respectively.  The recombinant xylanase showed stability cell cytoplasm (Jhamb and Sahoo 2012). However, effi - under harsh condition (high pH and temperature) and cient and functional expression of many xylanase genes high efficiency for biomass saccharification. However, is not possible with E. coli which may be due to repetitive the application of Pichia pastoris at large scale is limited appearance of rare codons and the requirement for spe- due to health and fire hazards of methanol (Ahmed et al. cific translational modifications (disulfide-bond forma - 2009). In the case of P. pastoris as expression system, tion and glycosylation) (Belancic et  al. 1995; Jhamb and lower protein yield was obtained while expressing mem- Sahoo 2012; Juturu and Wu 2012; Motta et al. 2013). One brane-attached protein or proteolytic degradation prone of the other important concerns associated with E. coli is protein and complex protein such as hetero-oligomers the presence of endotoxins (lipopolysaccharide) which (Ahmad et al. 2014). makes the protein purification process very tedious. Lactobacillus and Bacillus species are used for heterolo- Expression in filamentous fungi gous expression of xylanase than in E. coli. It is capable Filamentous fungi can be efficiently used for heterolo - of performing N-glycosylation, generally regarded as gous and homologous gene expression resulting in high safe (GRAS) due to the absence of endotoxins and their yield of recombinant gene products (Su et al. 2012; Motta secretory production is beneficial in industries (Bron et  al. 2013; Nevalainen and Peterson 2014; Nevalainen et  al. 1998; Subramaniyan and Prema 2002; Upreti et  al. et  al. 2018). Similar to yeast, it can regulate expression 2003; Juturu and Wu 2012). Zhang et al. (2010a, b) dem- yields with their own promoters and can provide eukary- onstrated the expression and characterization of the otic style post-translational modification of proteins such xylanase gene (xynB) from Dictyoglomus thermophilum as N-glycosylation, proteolytic processing, or formation Rt46B.1 in Bacillus subtilis system. The pH and tempera - of multiple disulfide bonds (Ahmed et al. 2009; Fleissner ture optima for the purified recombinant enzyme were and Dersch 2010; Landowski et al. 2015). Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 16 of 36 Ammonium sulfate precipitation followed by dialysis The application of fungi as an expression system also The crude xylanase preparation is subjected to different has advantages associated with cost-effectiveness of the ranges of ammonium sulfate concentration (30–90%) for overall process due to low-cost substrate and down- selection of suitable salt concentration for precipitation stream processing. Further, fungi have already been of the enzyme. The precipitated enzyme is then subjected subjected to many strain improvement procedures for to dialysis for removal of the salt. The crude xylanase enhanced production of xylanase. Therefore, the native obtained from Streptomyces P12-137 was subjected to xylanase expressing machinery can be efficiently used ammonium sulfate precipitation (40–90%) followed by for functional expression of a foreign xylanase gene dialysis. The purification fold of 4.18 was observed with from other sources. Xyn2 xylanase gene was expressed two different endoxylanase observed as F5 (65%) and F6 in T. reesei by homologous expression resulting in the (80%) with the specific activity of 45.4 U/mg and 36.5 U/ 1.61 g/L of xylanase 2 on glucose-containing medium (Li mg, respectively. This was also confirmed by HPLC anal - et  al. 2012). Godlewski et  al. (2009) demonstrated xyla- ysis. The purified enzyme was further characterized by nase B(XynB) gene expression in  T. reesei. Similarly, the incubating at different temperature and pH followed by expression of xylanase 2 (XYN2) and xylanase gene from analyzing the enzyme for xylanase activity. The optimum the thermophilic fungus Humicola grisea var. thermoidea pH and temperature of pH 7.0, 60  °C and 6.5, 60  °C, for and P. griseofulvum was expressed in Trichoderma reesei F5 and F6 xylanase, respectively, were obtained (Coman and Aspergillus oryzae, respectively (De Faria et al. 2002; et al. 2013). Motta et  al. 2013). Nevalainen and Peterson (2014) pre- Bhardwaj et  al. (2017) performed partial purification sented a comprehensive review on application of fila - of the crude xylanase obtained from Aspergillus oryzae mentous fungus as expression system and suggested that LC1 using ammonium sulfate (60%) precipitation fol- research is now focused on understanding the cellular lowed by dialysis against 50 mM acetate buffer (pH 5.0). mechanisms for better internal protein quality control The partially purified enzyme was further characterized and secretion stress. The better utilization of “omics” which showed stability over a wide pH range of 3 to 10 tools can help in improving the regulation of xylanase and thermal stability over the temperature range of 25 production using filamentous fungus as an expression to 60  °C. Similarly, Kumar et  al. (2018d) have demon- system. strated the purification and characterization of xylanase obtained from sea sediment bacteria using a combina- Strategies for enhanced purification tion of ammonium sulfate precipitation and dialysis. The and characterization of xylanase for industrial improvement in specific activity and characteristic prop - application erties of xylanase was observed. The major limitations of The microbial system produces a wide range of biochem - the precipitation are needed to remove salt from protein ical’s during different growth and development of the sample so further processing in the form of dialysis or microorganisms. These biochemical’s are enzymes, sec - chromatography is required. Further, for dialysis, there ondary metabolites, etc. which are of great importance is a need to have a better understanding of the protein to human applications. Similarly, enzymes are produced solubility. It is also stated that ammonium precipitation by microorganisms along with other enzymes or metabo- concentrates the protein rather than purifying it. Thus, lites. Therefore, purification is prerequisites for obtain - contaminant present in the crude sample may also be ing pure enzyme with minimum or no impurities (Zhang present along with the protein sample even after pre- et  al. 2012). The characterization of the purified enzyme cipitation and dialysis (Biosciences 2019). The xylanase such as evaluation of  temperature and pH optimum, is also concentrated or precipitated using trichloroacetic thermal and acid/alkali stability, role of  metal ions and acid (TCA) and acetone. However, the TCA may dena- inhibitors in regulation of enzyme activity, and substrates ture the protein; therefore, it is not advisable to use TCA specificity was performed  for selecting the suitable when the protein is required in the folded state (for activ- industrial process (Bhardwaj et al. 2019). There are differ - ity assay) and the toxicity of TCA also limits its applica- ent enzyme purification strategies for the xylanase such tions (Koontz 2014). as ammonium sulfate precipitation (salting in) followed by dialysis (salting out), gel permeation chromatography, Chromatography techniques for enhanced xylanase yield ion exchange chromatography, recently developed tech- employed for purification niques aqueous phase chromatography and ultrafiltration Usually, it has been observed that xylanase purifica - (Walia et  al. 2014; Guleria et  al. 2016b; Bhardwaj et  al. tion was performed by the multi-step process where 2019). Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 17 of 36 the concentration of protein using ammonium acetate/ i.e., aqueous two-phase system (Naganagouda and Muli- TCA/acetone precipitation or ultracentrifugation was mani 2008; Yasinok et al. 2010; Glyk et al. 2015). followed by a single step or series of chromatography Garai and Kumar (2013) purified alkaline xylanase from techniques. Yadav et  al. (2018) demonstrated the puri- Aspergillus candidus using aqueous two-phase system fication and characterization of extracellular xylanase (ATPS) composed of PEG 4000/NaH PO system. The 2 4 obtained from  A. kamchatkensis  NASTPD13 cultures. critical factors of ATPS such as PEG molecular weight, The crude xylanase was subjected to ammonium sulfate PEG and phosphate salt concentration using Box– (80%) precipitation followed by dialysis. The dialyzed Behnken design approach were used for the optimization sample was further subjected to Sephadex G100 column of enhanced xylanase purification. The optimum condi - chromatography. The fractions collected showing maxi - tion was PEG 4000 at 8.66% w/w with a high salt con- mum xylanase activity were concentrated and analyzed centration of 22.4 w/w that resulted in 8.41% purification by SDS-PAGE (MW obtained was 37  kDa). The two- fold. The enzyme was stable at alkaline pH and activity is 2+ step purification has led to increased xylanase activity by enhanced with Mn ions. Ng et al. (2018) demonstrated 11-fold with a 33 U/mg specific activity. The characteri - the recovery of xylanase from Bacillus subtilis fermenta- zation of purified protein showed pH and temperature tion broth with an alcohol/salt ATPS. The ATPS system optimum of 9.0 and 65 °C, respectively, and also retained consists of 26% (w/w) 1-propanol and 18% (w/w) ammo- more than 50% of its activity over a wide range of 6–9 nium sulfate resulting in 5.74 ± 0.33 purification fold and pH and 30–65  °C temperature. An insight into several yield of 71.88% ± 0.15. purification strategies employed for xylanase from differ - Gómez-garcía et  al. (2018) demonstrated purifica - ent microorganisms along with the process efficiency in tion of xylanase by Trichoderma harzianum using ATPS terms of recovery potential and kinetics property is tabu- with PEG/salt system. The PEG molecular weight, PEG, lated in Table 4. phosphate salt concentration, and salt conditions were Purification of endoxylanase obtained from Bacillus optimized. The best   enzyme recovery and  purifica - pumilus B20 was performed in three steps (Geetha and tion fold  of 62.5% and 10% respectively  was obtained Gunasekaran 2017). The first step was ammonium sulfate using 20.2% PEG 8000, 14.8% K HPO , and tie to a length 2 4 precipitation (60–80%) followed by FPLC using DEAE of 45% w/w. Bhardwaj et al. (2019) subjected crude xyla- Sepharose column as the second step and further sub- nase from Aspergillus oryzae LC1 to four different single- jecting the eluted sample onto a Sephacryl S-200 column step purification by ammonium sulfate precipitation, ion as the third purification step. At each step, the specific exchange, gel filtration chromatography and ATPS PEG/ activity was improved as compared to the crude enzyme Salt system. The xylanase purification using single-step by 5 to 14.8-fold with maximum 755.8 U/mg specific ATPS system resulted in highest purification yield (PY) of activity at the end of all the three purification steps. After 86.8% and 13-fold purification fold (PF) which was much the purification, the fractions showing maximum xyla - higher than other purification strategy, i.e., ammonium nase activity were subjected to xylanase assay and other precipitation (PY-21%, PF-4.1), anion exchange (PY- characterization studies such as SDS-PAGE, zymography, 31.9%, PF-3) and gel filtration (PY-78.7%, PF-6.6). temperature and pH stability. The SDS-PAGE and zymog - Therefore, ATPS exhibits several advantages over tra - raphy analysis showed the purified enzyme of ~ 85  kDa, ditional purification techniques, i.e., it requires low-cost i.e., endoxylanase (XylB). The purified enzyme was stable materials, low  energy consumption with high yield and in a pH range of pH 6.5 to 7.5 and the temperature range better resolution (Naganagouda and Mulimani 2008; of 20 to 50 °C. The purified enzyme was highly specific to Yasinok et al. 2010; Glyk et al. 2015). The ATPS method is different commercial and natural xylan substrate and has independent of protein concentration and does not affect the potential to generate xylooligosaccharides. the native property of protein (Iqbal et  al. 2016; Ram- akrishnan et al. 2016). Aqueous two‑phase system employed for purification of xylanase Structural properties of xylanase responsible The conventional multistep purification techniques are for thermal and pH stability required for industrial time consuming, which increases the cost of the overall application process and also results in loss of protein at each step The high stability of xylanase was due to the presence (Iqbal et al. 2016; Ramakrishnan et al. 2016). The 60–70% of intrinsic structural properties. The presence of extra of total processing cost in enzyme downstream process disulfide  and salt bridges, hydrophobic side chains, comes from the purification step (Loureiro et  al. 2017; and  N-terminal proline residues helps in  reduction Bhardwaj et  al. 2019). Therefore, several scientists sug - of conformational freedom of the protein structure. u Th s, gested a single step liquid–liquid fractionation technique, it help in providing more stability to protein at the higher Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 18 of 36 Table 4 Purification strategy employed for xylanase from different microorganisms Source organism Purification Specific activity Fold purification Recovery (%) K (mg/mL) V (μmol/mg/ Application of purified enzyme References m max methodology (IU/mg) min) Combined purification strategy Bacillus sp. SV-34S Ammonium sulfate 2803.1 10.62 88.0 3.7 133.33 IU/mL Paper and Pulp industry Mittal et al. (2013) precipitation (80%) Carboxymethyl 3417.2 12.94 13.44 Sephadex C-50 cation exchange chromatography Bacillus sp. GRE7 Ammonium sulfate 191.1 3.9 71 2.23 296.8 IU/mg Eucalyptus kraft pulp bio-bleaching Kiddinamoorthy et al. (40–80%) (2008) DEAE-Cellulose 582.9 11.9 48 Sephadex G-75 1392.6 28.5 27 Arthrobacter sp. Ammonium sulfate 162 2 74 0.9 3571 – Khandeparkar and Bhosle (2006) Sephadex G-200 282.6 3.5 62 DEAE-Sepharose FF 444.2 5.5 49 CM-Sepharose FF 1697.7 21 14 Thermotoga ther- Ni-affinity chroma- 192 6.9 82.3 1.8 769 XOS generation Shi et al. (2014) marum tography Glaeocola mes- Ammonium sulfate 77 9.1 17.4 1.22 98.31 XOS generation, Sea and saline Guo et al. (2009) ophila KMM 241 Dialysis food processing, bakery indus- Ni -NTA Agarose tries resins Streptomyces oliva- Ammonium sulfate 37.35 ± 1.33 1.045 ± 0.002 60.69 ± 2.38 8.16 250.01 High sugar yield and bioethanol Sanjivkumar et al. ceus (MSU3) fractionation generation ability using lignocel- (2017) lulosic biomass Dialysis 82.40 ± 2.50 2.298 ± 0.021 38.29 ± 1.53 DEAE–cellulose 116.98 ± 2.28 3.260 ± 0.024 28.15 ± 1.87 column Sephadex-G-75 153.11 ± 2.11 4.270 ± 0.026 15.57 ± 0.85 column Penicillium gla- Ammonium sulfate 291.78 3.25 84.19 1.2–5.3 212.10–393.17 Purified enzyme suitable for animal Knob et al. (2013) brum fractionation feed additives, clarification, and maceration of juices and wines Molecular exclusion 457.89 5.10 76.92 chromatography (Sephadex G-75 column) Trichoderma Dialysis followed Xyl I-1257.7 Xyl I, II-1.9 Xyl I-62.7 Xyl I-1.6–14.5 Xyl I-462.2–2680.2 XOS generation da Silva et al. (2015) inhamatum by ion exchange Xyl II- Xyl II-3.7 Xyl II-4.0–10.7 U/mg chromatography 1216.4 Xyl II-1972.7–4553.7 (DEAE Sephadex U/mg A-50 column) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 19 of 36 Table 4 (continued) Source organism Purification Specific activity Fold purification Recovery (%) K (mg/mL) V (μmol/mg/ Application of purified enzyme References m max methodology (IU/mg) min) Chrysoporthe Q Sepharose anion – P2-1.2 P2-13.4 P2-1.81 – Efficient saccharification of sugar - de Sousa et al. (2017) cubensis exchange column P3-1.4 P3-1.3 P3-1.18 cane bagasse followed by Sephacryl S-200 gel filtration column Myceliophthora Ni Sepharose resin 102.2 44 7 13.4 ± 1.5 274.5 ± 1.0 Pulp bleaching de Amo et al. (2019) heterothallica containing His- F.2.1.4 Trap HP column Aspergillus flavus Ammonium sulfate 621.4 2.7 46.7 – – Efficiently hydrolyzed pretreated Chen et al. (2019) fractionation corncobs for generation of XOS (40–60%) Gel filtration (HiPrep 838.2 3.7 34.8 16/60 Sephacryl S-100 HR column) chromatography Penicillium chrys- Ion exchange chro- 438.3 9.8 49.3 2.3 mM 731.8 U/mg Beverage, bakery, and feed indus- Terrone et al. (2018) ogenum matography (CM try. For production of xylooligo- Sephadex C-50 saccharides and bioethanol column) Size exclusion 834.2 18.7 31.1 chromatography (Sephadex G-100 column) Single step purification strategy −1 Streptomyces Ammonium sulfate F5-45.44 4.18 F5-60.63 F5-0.2012 F5-0.4742 s Efficient XOS generation Coman et al. (2013) −1 P12-137 precipitation fol- F6-36.48 F6-73.02 F6-0.0388 F6-0.6314 s lowed by dialysis Sorangium cellulo- Ni-affinity followed 4.11 4.03 43.84 38.13 10.69 Hydrolysis of xylan rich substrates Wang et al. (2012) sum So9733-1 by dialysis and and food industries concentration Aspergillus tamarii Single step purifica- 1215.89 7.43 36.72 7.59–8.13 1178.56–1330.20 XOS generation Heinen et al. (2018) Kita tion carboxym- ethyl-cellulose (CM-cellulose) chromatography Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 20 of 36 Table 4 (continued) Source organism Purification Specific activity Fold purification Recovery (%) K (mg/mL) V (μmol/mg/ Application of purified enzyme References m max methodology (IU/mg) min) Scytalidium ther- Ammonium sulfate 125.9 2.5 52 2.4 168.6 IU/mL Agricultural biomass hydrolysis for Kocabacs et al. (2015) mophilum ATCC precipitation application in bioethanol refinery No. 16454 (50%) ATPS (7% Triton 79.8 2.7 79 X-114 top phase) 10 kDa molecular 841.1 4.3 25 weight cut-off (MWCO) Aspergillus oryzae Ammonium sulfate 631 4.1 21 0.2 172.2 XOS generation Bhardwaj et al. (2019) LC1 Precipitation fol- lowed by dialysis Anion exchange 469 3 31.9 Chromatography (DEAE-Sephadex A-50) Gel Filtration 101.5 6.6 78.7 Chromatography (Sepharose G-100) ATPS with Triton 508.9 3.3 69.4 X-114 (5% v/v) ATPS with PEG 2004.3 13 86.8 (22.5% MgSO Salt 11.3% PEG 8000) Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 21 of 36 temperature (Turunen et al. 2001; Chen et al. 2015). Dif- respect to volumetric productivity, which suggested that ferent structural modifications such as high Thr/Ser ratio remarkable reduction in cost of enzyme production may and high charged residues, i.e., Arg, cause enhanced be observed under optimized conditions. Thus, based on polar interaction and improved stabilization of the alpha- the above studies, we can suggest that xylanase produc- helix region and secondary structures (Hakulinen et  al. tion can be based on the cost of substrate and consuma- 2003). The xylanase protein has a large number of ion ble, along with the cost of each step involved in upstream pairs/aromatic residues on the surface of protein result- and downstream processing. Therefore, utilizing cheap ing in enhanced interactions (Polizeli et  al. 2005; Chen raw materials, less number of steps during upstream et  al. 2015). The low average protein rigidity i.e. low B and downstream process (such as single step purifica - factor, low flexibility results in  high rigidity at extreme tion instead of multistep process) can help in keeping the physical conditions (Xie et  al. 2014). The presence of enzyme production cost as low as possible. divalent metal ions and removal of N or C terminal dis- ordered residues protect xylanase from heat and protease Xylanase employed as a greener tool in different inactivation (Andrews et al. 2004; Chen et al. 2015). The industries presence of carbohydrate-binding modules (CBM22 and Xylanase with such unique characteristics of thermo- CBM9) at N or C terminal often imparts heat stabil- alkali tolerant nature has a diverse range of application ity to xylanase. The pH stability of the xylanases is often in different industries such as paper and pulp, deinking, affected by the presence of several amino acids near the biomass utilization and food feed industries (Fig. 6). catalytic residues (Singh et al. 2019). Xylanase employed in the food and feed industry Cost estimation of the xylanase production Bakery Polizeli et al. (2005) suggested that 20% of the total global The xylanase finds application in food industries such enzyme production is from biomass hydrolysis enzymes, as bakery. The bread is made up of wheat consisting i.e., xylanase, cellulase and pectinases. An extensive of hemicelluloses such as arabinoxylan. The xylanase study on cost involved in each step of xylanase produc- can solubilize the water unextractable arabinoxylan tion at industrial scale is unavailable on public domain. into water-extractable arabinoxylan (Courtin and Del- Klein-Marcuschamer et  al. (2012) performed a study on cour 2002). This help in uniform water distribution and the cost analysis of application of enzymes during the lig- improvement in gluten network formation throughout nocellulosic biomass based biofuel production and sug- the dough. The addition of xylanase improves the rheo - gested breakdown of the operating cost (annual) in their logical properties of dough such as softness, extensibil- enzyme production facility. They suggested percentage ity, and elasticity along with bread-specific volume and of cost involved for each component, i.e., raw materials crumb firmness (Harbak and Thygesen 2002; Camacho (28%), labor (7%), transportation (1%), consumables (4%), and Aguilar 2003; Butt et al. 2008). The breakdown prod - utilities (10%), facility dependent (48%), and waste treat- ucts of arabinoxylan, i.e., arabino-xylooligosaccharides in ment (2%). This clearly shows that maximum contribu - bread have its health benefits (Polizeli et al. 2005; Bajpai tion of 48% comes from the capital investment followed 2014). by cost of substrate (28%). Klein-Marcuschamer et  al. Butt et  al. (2008) demonstrated the role of GH11 (2012) also suggested the baseline production cost of endoxylanases from B. subtilis in solubilizing the ara- hydrolysis enzyme as $10.14/kg. binoxylan. This increases the viscosity and volume of Da Gama Ferreira et al. (2018) performed techno-eco- dough and decreases gluten agglomeration and dough nomic analysis of the β-glucosidase enzyme production firmness resulting in the development of uniform and from E. coli on industrial scale. They showed  major cost fine crumbs. GH11 xylanase (0.12 U/g flour) from Peni - during industrial production are facility dependent (45%) cillium occitanis Pol6 resulted in improvement of bread- followed by raw materials (25%) and consumables (23%), making process such as the decrease in water absorption that  are similar to observations made by  Klein-Marcus- (8%) and an increase in dough rising (36.8%), volume chamer et al. (2012). Capital investment/facility-depend- (17.8%), specific volume (34.9%) and cohesiveness. The ent cost is required for development of infrastructure bread has improved rheological and sensory properties (i.e., equipments), insurance, maintenance and depre- (texture, taste, flavor, softness, and overall acceptability). ciation. This upstream and downstream process during Low springiness and gumminess were observed in the enzyme production involves the cost on part of capital bread prepared using xylanase (Driss et al. 2013). Partially investment along with the cost of consumables and utili- purified microbial xylanase was used by Ghoshal et  al. ties. da Gama Ferreira et  al. (2018) performed sensitiv- (2013) to produce whole‐wheat bread with better sen- ity analyses of process scale, inoculation volume with sory properties (brighter color). The addition of xylanase Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 22 of 36 Fig. 6 Xylanase as a greener tool in different industries also resulted in increased specific volume, and shelf life, Streptomyces sp was used for the clarification of orange, with lower firmness and reduced staling during storage. mousambi, and pineapple with 20.9%, 23.6% and 27.9% Panzea, new generation xylanase obtained from Bacillus clarity, respectively (Rosmine et  al. 2017). Immobilized Licheniformis, can help in improving dough properties at xylanase obtained from Bacillus pumilus VLK-1 was low enzyme dosage. It helps in achieving the desired tex- used for orange (29%) and grape juice (26%) enrichment ture, appearance, loaf volume and crumb structure (Baj- (Kumar et  al. 2014). Xylanase immobilized on 1,3,5-tri- pai 2014). Similarly, recombinant xylanase (r-XynBS27) azine-functionalized silica-encapsulated magnetic nano- obtained from Pichia pastoris (xynBS27 gene from Strep- particles was reported to clarify the three different types tomyces sp. S27) used as an additive during bread-making of fruit juices after five hours of incubation at 50  °C process. The recombinant xylanase resulted in improve - (Shahrestani et al. 2016). Partially purified xylanase from ment in a specific volume and reducing sugar content Streptomyces sp AOA40 was used in fruit juice industry with a decrease in firmness, consistency, and stiffness (De for increased clarity of juices from apple (17.8%), orange Queiroz Brito Cunha et al. 2018a, b). (18.4%) and grape (17.9%) (Adigüzel and Tunçer 2016). Glutaraldehyde-activated immobilized xylanase was Fruit juice clarification used for the clarification of tomato juice. Xylanase from The enzymatic process in fruit juice extraction and clari - P. acidilactici GC25 was used to treat the kiwi, apple, fication is widely used. Raw juices of fruit contain poly - peach, orange, apricot, grape, and pomegranate in which saccharides such as cellulose, hemicellulose, starch pectin increase in the amount of reducing sugar was observed and surface-bound lignin and decrease the quality of the along with the decrease in turbidity of the juice (Adiguzel juice, e.g., hazy color and high viscosity (Danalache et al. et al. 2019). 2018). The use of enzymes decreases the viscosity and avoids the formation of clusters, by removing the sus- Animal feed pended and undissolved solid using centrifugation and Xylanases plays an important role in animal feed by filtration methods. This increases the clarity, aroma, and breaking the feed ingredient arabinoxylan and reduces color of the juice (Danalache et  al. 2018). Xylanase from the raw material viscosity. Aspergillus japonicus C03 with Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 23 of 36 good endoxylanase and cellulase production ability with xylanase using agro-residues active at high temperature high stability in the presence of goat ruminal environ- 60 °C and pH 6–10 and was utilized for bio-bleaching of ment showed ruminant feed applications (Facchini et  al. kraft pulp (Azeri et  al. 2010). Paenibacillus campinasen- 2011). A number of studies reported the availability of sis BL11 xylanase pretreatments showed the increased distillers dried grains with soluble (DDGS) to be utilized brightness and viscosity of hardwood kraft pulp (Ko et al. in animal feeds and use of exogenous xylanase in poul- 2010). S. thermophilum xylanase active at high tempera- try diets to treat the higher fiber content (Pirgozliev et al. ture (50–70  °C) was used for the bleaching of bagasse 2016; Whiting et al. 2019). The exogenous enzymes effec - pulp (Joshi and Khare 2011). T. lanuginosus VAPS24 tively improved the nutritional value of co-products of xylanase was stable at wide range pH that can be use- bioethanol as reported previously with DDGS obtained ful in both alkaline and acidic bioprocesses (Kumar and from corn (Liu et al. 2011). Xylanases have been involved Shukla 2018). An alkaliphilic Bacillus liceniformis Alk-1 in animal feed over decades, as it reduces the viscos- xylanase was utilized in a purified form for the enzy - ity of digesta in poultry. Xylanase addition showed the matic pretreatment on eucalyptus kraft pulp bleach- weight gain improvement and enhanced feed conver- ing (Raj et  al. 2018). The xylanase preparation obtained sion ratio because of the improvement in the arabinoxy- from white-rot fungi, S. commune ARC-11 was capable of lan digestibility in monogastric animal diets (Paloheimo ethanol soda pulp pre-bleaching from Eulaliopsisbinata et  al. 2010; Van Dorn et  al. 2018). Xylanase utilized as a (Gautam et  al. 2018). The paper  manufacturing units dietary supplement for the nutrients digestibility, digesta of various countries, i.e., Japan. South America, North viscosity growing pigs fed corn intestinal morphology America and Europe are slowly replacing chemical pulp diet based on soybean meal was reported by Passos et al. bleaching by xylanase mediated pulp bleaching. Canada (2015). ECONASE XT a well-known commercial endo- is known to be the leading producer of pulp and they are 1,4-β-xylanase which has been used as feed additives for bleaching more than 10% its pulp via xylanase (Dhiman chicken fattening, weaned piglets and fattening for pigs et al. 2008a). In addition to that, several reports also sug- (Rychen et al. 2018). gest that the xylanase enzyme-mediated pretreatment can help in generation of cellulosic nanofibres (CNF) Xylanase in paper and pulp industries with improved crystallinity from unbleached bagasse and Bio‑bleaching eucalyptus pulp (Nie et  al. 2018; Zhang et  al. 2018; Tao The process of removal of lignin from wood pulp to et  al. 2019). Zhang et  al. (2018) suggested that applica- produce bright and completely white finished paper tion of commercial Novozyme X2753 can simplify the is known as bleaching (Beg et  al. 2001). Traditionally, CNF’s production and purification process. Tao et  al. chemical bleaching agents (such as chlorine) were used (2019) demonstrated that xylanase can directly act on for bleaching (Subramaniyan and Prema 2002). The use the unbleached pulp, where it acts on the covalent bond of ligno-hemicellulolytic enzymes for bleaching has between hemicellulose molecule and hydrogen bond gained impetuous all over the world. Xylanases are capa- between hemicelluloses and cellulose. The presence of a ble of hydrolyzing xylan which is linked to the cellulose small amount of hemicelluloses in cellulose nanofibrils and lignin of the pulp fiber. Thus, xylan disruption will increases light blockage efficiency and subsequently the eventually lead to the separation between these compo- energy storage capacity of solar cells. Thus, xylanase- nents, enhance swelling in the fiber wall, and improve mediated bio-bleached pulp acts as a potential substrate lignin extraction from the pulp (Thomas et  al. 2015). for flexible solar cells. uTh s, xylanase in combination with lignin-degrading enzyme help in increasing the brightness of pulp (Vii- Deinking of waste paper kari et al. 1994; Sunna and Antranikian 1997; Pérez et al. The dislodgement of ink from the waste used paper is 2002; Motta et  al. 2013). The exposures of the cellulose required for its recycling and reuse. Chemical-based fiber to enzymatic pulping enhance the bonding forces methods involving chlorine or chlorine-based deriva- of paper and improve paper strength via degradation of tives, ClO , NaOH, NaCO, H O, Na SiO , have been 3 2 2 2 2 xylan and removal of lignin during enzymatic treatment used for removing ink from the paper. This resulted in (Lin et  al. 2018). The enzymatic system has been highly generation of hazardous effluents and required tedious selective, non-toxic, environmentally friendly approach treatment before disposal to the environment (Maity for bio-bleaching (Bajpai 2012). et  al. 2012). The enzyme-based methods utilizing xyla - Paper and biomass pulp processing takes place at vary- nase and laccase have been suggested for the removal of ing pH and temperature. Therefore, thermo-alkali stable ink from paper and pulp industries effluents (Chandra xylanases are required for the bio-bleaching. An alkaliph- and Singh 2012; Dhiman et al. 2014). ilic Bacillus strain produced thermoactive cellulase-free Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 24 of 36 Virk et  al. (2013) explored the deinking efficiencies of Garg et  al. (2013) demonstrated the application of bacterial alkalophilic laccase and xylanase along with alkalo-thermostable xylanase from Bacillus pumilus ASH physical deinking methods such as microwave and ultra- in bioscouring of jute fabric. The oven-dried jute fabric sound for recycling of waste paper. The combination of when incubated with a small dose of 5  IU/g xylanase at xylanase and laccase enzymes showed an increase in 55  °C for 2  h resulted in an increase in 4.3% whiteness brightness of different waste pulp old newsprint pulp and 10.7% brightness of fabric. Further, it also helped in (21.6%), inkjet print pulp (4.1%), laser print pulp (3.1%), decreasing in yellowness of fabric by 5.57%. Similarly, magazine pulp (8.3%), and xerox paper pulp (1.9%) only. xylanase from Bacillus pumilus was studied for enzy- Gupta et  al. (2015) reported that synergistic action matic desizing of cotton and micropoly fabrics (Battan of xylanase and laccase enzyme (co-cultivation of Bacillus et al. 2012). The enzymatic desizing with enzyme load of sp. and B. halodurans FNP135) resulted in improvement 5  IU/g at pH 7.0, temperature 60  °C for 90  min resulted of physical properties like freeness, breaking length, burst in improved whiteness of 0.9% with respect to the chemi- factor and tear factor by 17.8%, 34.8%, 2.77%, and 2.4%, cal process. The addition of surfactant such as EDTA respectively, of old newspaper. The appearance of the improved the desizing and bioscouring efficiency (Loson - newspaper was also improved with an increase in 11.8% czi et al. 2005; Battan et al. 2012; Garg et al. 2013). brightness and 39% whiteness. The effective dose of com - The synergistic action of xylanase and pectinase mercial cellulase and xylanase from Bacillus halodurans enzyme was used for scouring of cotton fabrics. The bios - TSEV1 for removal of ink was determined at 1.2. U/mg couring was performed with 5.0  IU xylanase and 4.0  IU (each enzyme) by Kumar and Satyanarayana (2014). The pectinase from Bacillus pumilus  strain AJK (MTCC cellulase and xylanase complex obtained from Escheri- 10414) along with surfactants such as 1.0  mM EDTA chia coli SD5 facilitated the reduction in hexenuronic and 1% Tween-80 at high pH 8.5 for 1  h at 50  °C. They acid (Hex A) and kappa number, increase in brightness observed improvement in whiteness, brightness, and (10%) and tear strength of recycled paper (Kumar et  al. reduction in yellowness by 1.2%, 3.2%, and  4.2% respec- 2018c). tively  that is better  in comparison to chemical-based alkaline scouring method (Singh et  al. 2018). El et  al. (2018) reported improvement in desizing, bioscouring Xylanase employed in textile industries and bio-finishing efficiency using xylanase obtained from The textile processing can be broadly divided into desiz - T. longibrachiatum KT693225 without any requirement ing, scouring and bleaching. Desizing involves removal of additives. of adhesive material from plant fibers and scouring to remove the inhibitory material from desized fibers Xylanase employed in chemical (Hartzell et  al. 1998; Dhiman et  al. 2008b). The conven - and pharmaceutical industries tional method used for desizing and scouring involves The non-digestible sugar molecules together form oli - the application of high temperature under the influence gomers known as xylooligosaccharides, which are made of oxidizing agents in the alkaline system. This method up of xylose monomers (Vazquez et  al. 2000). XOS has is not only chemical intensive but also non-specific that various applications in biotechnology, pharmaceuti- causes hamper to the useful cellulosic fractions compro- cal, food and feed industries (Chang et  al. 2017). XOS mising the overall strength of the textile fibers. Therefore, plays a vital role as prebiotic as it is not hydrolyzed application of highly thermo-alkali stable cellulase-free or absorbed in the gastrointestinal tract. uTh s, XOS xylanolytic enzyme can efficiently be used for desizing selectively stimulates the growth of important gastro- and scouring (Csiszár et  al. 2001; Losonczi et  al. 2005; intestinal microorganisms regulating the human diges- Dhiman et al. 2008b; Bajpai 2014). tive health (Roberfroid 1997; Collins and Gibson 1999; Dhiman et al. (2008b) demonstrated the application of Vazquez et al. 2000). The potential of XOS as an efficient alkalo-thermophilic xylanase from Bacillus stearothermo- feed alternative is established by the fact that it  help in philus SDX for processing of cotton and microply fabrics. cholesterol reduction, inhibit starch retro-gradation, The desizing and bioscouring treatments were performed improve the bioavailability of calcium thus improving using 5 g/L of xylanase at 70 °C, pH 9.5, for 90 min. This the nutritional and sensory properties of food (Voragen resulted in weight loss for 0.91% in microply and 0.83% 1998; Motta et al. 2013). XOS has shown the application in cotton with overall whiteness index of 11.81% for cot- in pharmaceutical sectors due to its immunomodulatory ton and 52.15% for micropoly. The processed fabric has (Chen et  al. 2012), anti-cancerous (Gupta et  al. 2018), increased tensile strength (1.1–1.2%) and tearness value anti-microbial, antioxidant (Kallel et  al. 2015b), anti- (1.6–2.4%) as compared to control. allergy, anti-inflammatory (Aachary and Prapulla 2011), Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 25 of 36 and anti-hyperlipidemic activity (Li et  al. 2010). XOS hydrolysis of the pretreated biomass for the conversion have also shown phyto-pharmaceutical and feed applica- of complex carbohydrate polymer of LCB to the simple tions such as growth regulatory activity in aquaculture monomers which will be further converted to ethanol by and poultry. These properties may be due to the presence fermentation. The xylanolytic enzyme in combination of uronic substituents in acidic oligosaccharides. with cellulolytic enzyme plays an important role in the The process of XOS synthesis involves the physi - hydrolysis process. cal (autohydrolysis), chemical (hydronium ions gener- Several reports suggest that xylanase obtained from sev- ated by water autoionization and in  situ organic acids) eral microorganisms plays an important role in sacchari- or enzymatic hydrolysis (xylanase or β-xylosidase) of fication of LCB for lignocellulosic-based biorefinery (Hu hemicellulose-rich agricultural wastes (Aachary and et  al. 2011; Choudhary et  al. 2014; Ramanjaneyulu et  al. Prapulla 2011). Several reports suggested that XOS can 2017; Basit et  al. 2018). Hydrolysis and fermentation are be enzymatically produced from different agro-residues important steps in biomass to bioethanol generation. Ini- such as hardwoods (Huang et  al. 2016), straws (Gullón tially, several groups demonstrated separate hydrolysis of et  al. 2008; Kallel et  al. 2015a; Moniz et  al. 2016) corn biomass followed by fermentation (SHF). SHF is a time- cobs (Chapla et  al. 2013; Gowdhaman and Ponnusami consuming process and thus increases the overall cost of the 2015), bran (Otieno and Ahring 2012), sugarcane bagasse process. Later on, different integrated process (combined (Jayapal et al. 2013) and bamboo (Xiao et al. 2013) using hydrolysis and fermentation) have been developed such as microbial xylanases. simultaneous saccharification and co-fermentation (SSCF), Alkaline xylanase from Bacillus mojavensis A21 utilized simultaneous saccharification and fermentation (SSF), and corncob xylan for the release of xylotriose and xylobiose consolidated bioprocessing (CB) (Malhotra and Chapad- (Haddar et  al. 2012). Bacillus aerophilus KGJ2 xylanase gaonkar 2018). These strategies resulted in an enhancement showed efficiency toward XOS synthesis, e.g., xylobiose, in reaction rates and ethanol yields (Eklund and Zacchi xylotriose, and xylose after hydrolysis of xylan (Gowdha- 1995; Sun and Cheng 2002). Bibra et  al. (2018) showed man et  al. 2014). A cellulase free xylanase (EX624) from thermostable xylanase production using Geobacillus sp. Streptomyces sp. CS624 produced xylose, xylobiose and DUSELR13, which is applied further for ethanol generation xylotriose with commercial beech wood xylan and wheat from LCB. SSF Geobacillus sp. DUSELR13 and Geobacillus bran (Mander et al. 2014). Using deoiled Jatropha curcas thermoglucosidasius are co-cultured for SSF of prairie cord seed cake as substrate, Sporotrichum thermophile xyla- grass (PCG), and corn stover (CS). The SSF resulted in 3.53 nase was produced which showed the efficiency to pro - and 3.72 g/L ethanol from PCG and CS, respectively. duce XOS by the hydrolysis of oat spelt xylan, with 73% Hu et  al. (2011) suggested that xylanase causes fiber xylotetraose, 15.4% xylotriose and 10% xylobiose (Sadaf swelling improving porosity that helps in improving and Khare 2014). Xylanase obtained from the mixed the accessibility of cellulose. To ferment both cellulose- microbial culture of Cellulomonas uda NCIM 2523 and derived hexoses (C6) and xylan-derived pentoses (C5), Acetobacter xylinum NCIM 2526 using Prosopis juliflora simultaneous saccharification and co-fermentation showed the potential to produce XOS with probiotic (SSCF) was introduced which causes ethanol production activity from beech wood xylan (Anthony et  al. 2016). using single microorganisms co-cultured with cellulase A xylanase gene PbXyn10A isolated from Paenibacil- and xylanase producing strain. Yasuda et al. (2014) dem- lus barengoltaii cloned in E. coli showed 75% XOS yield onstrated bioethanol generation by SSCF of anhydrous from xylan extracted from raw corncobs (Liu et al. 2018). ammonia-pretreated  Pennisetum purpureum Schumach The hydrolysis of xylan using xylanase from Pichia stipitis (Napier grass) using Escherichia coli KO11 and Saccha- produced 2% XOS consisting of xylotetraose 14%, xylotri- romyces cerevisiae cellulase, and xylanase. SSCF for 96 h ose 49% and xylobiose 29% (Ding et  al. 2018). Bhardwaj was reported to have a maximum 74% ethanol yield as et al. (2019) demonstrated the partially purified xylanase compared to theoretical yield calculated based on glucan obtained from Aspergillus oryzae LC1 resulted in the and xylan yield of 397 mg/g and 214 mg/g, respectively. generation of xylobiose, xylotriose, and xylotetraose. Bondesson and Galbe (2016) designed experimen- tal setup of SSCF for ethanol production from steam- Xylanase employed in biorefinery pretreated, acetic acid-impregnated wheat straw using Efficient conversion of lignocellulosic biomass (LCB) into a pentose fermenting S. cerevisiae KE6-12b strain. The fuel-grade ethanol has become a world priority for pro- highest 37.5  g/L ethanol concentration with 0.32  g/g ducing environmentally friendly renewable energy at a ethanol yield was obtained based on the glucose–xylose reasonable price for the transportation sector. The pro - available in the pretreated wheat straw. Shariq and Sohail cess of bioconversion of lignocellulosic biomass requires (2018) demonstrated that yeast strain Candida tropicalis Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 26 of 36 MK-160 can help in xylanase and endoglucanase produc- having ligno-hemicellulolytic enzymes having the capa- tion as well as ethanol production. Therefore, it can be bility along with ethanol generating potential. Shen et al. potentially used for SSCF involves single microorganism. (2012) engineered a thermostable self-splicing bacterial The consolidated processing or simultaneous deligni - intein-modified xylanase for consolidated lignocellu - fication, saccharification, and fermentation involve the losic biomass processing. Sun et al. (2012) demonstrated cultivation of ligno-hemicellulolytic enzyme-producing expression of recombinant Saccharomyces cerevisiae strains along with ethanol-producing strain in a reactor. strain having an engineered minihemicellulosome. It It may be monoculture or co-culture of different microor - has the capability of converting xylan directly to ethanol. ganisms. It will help to decrease the overall process cost Horisawa et  al. (2019) suggested direct ethanol produc- required for bioreactor and operation of different enzyme tion from lignocellulosic materials by consolidated bio- production and ethanol generation (Chadha et al. 1995). processing using the mixed culture of wood rot fungi, i.e., To design a monoculture-based consolidated pro- Schizophyllum commune, Bjerkandera adusta, and Fomi- cessing, different engineered microorganisms are used topsis palustris. Fig. 7 Future prospect for development in area of xylanase production using conventional and advanced approaches Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 27 of 36 Commercial xylanase enzyme and their application bioinformatics tools to develop different approaches for The xylanase enzyme is commercially employed in sev - enhanced xylanase production. The combination of new eral industries such as pulp bleaching, food, feed, and technology such as synthetic biology (DNA oligo-synthe- brewing. The major application of the xylanase is in pulp sis) and conventional recombinant DNA technology can bleaching and is produced by different companies around be used for attaining the objective of high xylanase pro- the world with various trade name such as Bleachzyme duction with desired industrial properties (Fig.  7). How- (Biocon, India), Cartzyme (Sandoz, US), Cartzyme MP ever, limitations associated with mimicking the natural (Clarient, UK), Ecozyme (Thomas Swan, UK), Irgazyme system into synthetic system need to be taken care before 10 A & Irgazyme 40–4× (Genercor, Finland), Ecopulp full-scale applications. Also, the ethical, socio-economic (Alko Rajamaki, Finland), VAI Xylanase (Voest Alpine, and health concerns need to taken care before  commer- Austria), and Rholase 7118 (Rohm, Germany). Xylanase cial exploitation of the developed strategies. is commercially produced by several international indus- tries for its application in food and feed industries. San- Conclusion kyo from Japan, Ciba Giegy from Switzerland produces The enzymatic breakdown of the xylan into its constitu - xylanase as trade name Sanzyme, and Albazyme-10A, ent component requires the synergistic action of xyla- respectively, and has been used commercially in food and nases and other debranching enzymes. The key enzyme baking industries. A Danish firm Novo Nordisk, produces used for xylan hydrolysis is endo-1,4-β-xylanase that three commercial xylanases namely Pulpzyme (HA, HB, cleaves β-1,4-glycoside linkage of xylan. The xylanase HC), Biofeed (Beta, plus) and Ceremix and used in pulp can be grouped under different GH families with major bleaching, feed and brewing industries, respectively xylanases from GH10 or GH11 families, followed by (Walia et al. 2017). An American firm Alltech, Inc., com - GH5, GH7, GH8 and GH43. The xylanase enzyme acts mercially produces xylanase with trade name Allzym PT as a “Green” alternative to already existing industrial and Fibrozyme and has been used for the upgrading the processes for processing of xylan to different industrially animal feed. A Japanese firm named Amano Pharmaceu - important product such as paper, textile, food, feed, phar- tical Co, Ltd. produced xylanase enzyme named Amano maceuticals, and biofuels. The application of xylanases 90 and it has been used in food, feed and pharmaceuti- in the production of the above-mentioned products can cal industries. Most of the commercial xylanases are regulate the overall economics of the process. Therefore, produced by fungal source due to its high production already existing method can be further improved or new potential. strategies may be developed for enhanced and cost-effi - cient production of xylanase with desired characteristics. Further, it is often observed that native enzyme cannot Challenges and future trends in commercial meet the industrial process requirement; thus, the com- production, purification and application bination of already existing technology with new tech- of xylanase nology such as synthetic biology (DNA oligo-synthesis), The search of super xylanase is still on, therefore, search - rational engineering and directed evolution can be used ing for new microbial source with the ability to produce for attaining the objective of high xylanase production highly active and stable xylanase is going on around the with desired industrial properties. world. The strains isolated from different extreme habitat can be of potential applications as these strains already possesses the ability to withstand different stress such Abbreviations as high temperature and pH variations. The selection LCB: lignocellulosic biomass; EC: enzyme commission; HMWLI: high-molecular weight with low isoelectric point; LMWHI: low-molecular weight with high of such thermal and pH tolerant strains and subjecting isoelectric point; CAZy: carbohydrate-active enzyme database; NCBI: National them to different optimization strategies for enhanced Centre for Biotechnological Information; GH: glycoside hydrolase; XOS: xylo- xylanase production can be one alternative. The advance oligosaccharides; X2: xylobiose; X3: xylotriose; X4: xylotetraose; CNB: catalytic nucleophile/base; CPD: catalystic proton donor; Asp: aspartic acid; Glu: gluc- ment in biotechnological tools and techniques (Recom- tamic acid; SmF: submerged fermentation; SSF: solid-state fermentation; CMC: binant DNA technology or genetic engineering) provides carboxymethyl cellulose; OFAT: one factor at a time; CCD: central composite an opportunity to select the gene responsible for xylanase design; ANOVA: analysis of variance; RSM: response surface methodology; GRAS: generally regarded as safe; TCA: tr ichloroacetic acid; SDS–PAGE: sodium production that can be isolated and efficiently transferred dodecyl sulfate-polyacrylamide gel electrophoresis; DEAE: diethylaminoethyl; to the expression system. These expression systems can FPLC: fast protein liquid chromatography; ATPS: aqueous two-phase system; be regulated for enhanced production of xylanase with PEG: polyethylene glycol; DDGS: distillers dried grains with soluble; SSCF: simultaneous saccharification and co-fermentation; SSF: simultaneous sac- desired property for specific industrial applications. The charification and fermentation; CB: consolidated bioprocessing; PCG: prairie availability of a high amount of genomics, proteom cord grass; CS: corn stover. ics and metabolomics data can be used via different Bhardwaj et al. Bioresour. Bioprocess. (2019) 6:40 Page 28 of 36 Acknowledgements Ahmed S, Riaz S, Jamil A (2009) Molecular cloning of fungal xylanases: an The authors are thankful to the Department of Biotechnology, Government of overview. Appl Microbiol Biotechnol 84:19–35 India for providing the financial support (Grant Nos. BT/304/NE/TBP/2012 and Akila G, Chandra TS (2003) A novel cold-tolerant Clostridium strain PXYL1 BT/PR7333/PBD/26/373/2012). NB is thankful to the University Grants Commis- isolated from a psychrophilic cattle manure digester that secretes ther- sion for providing fellowship for doctoral studies. BK is thankful to Jawaharlal molabile xylanase and cellulase. FEMS Microbiol Lett 219:63–67 Nehru memorial Fund and CSIR for providing scholarship for doctoral studies. Al Balaa B, Wouters J, Dogne S et al (2006) Identification, cloning, and expression of the Scytalidium acidophilum XYL1 gene encoding for an Authors’ contributions acidophilic xylanase. Biosci Biotechnol Biochem 70:269–272. https :// NB and BK developed the manuscript and wrote the manuscript under guid- doi.org/10.1271/bbb.70.269 ance of PV. PV provided time to time scientific and technical comments to Alam M, Gomes I, Mohiuddin G, Hoq MM (1994) Production and characteriza- enhance the quality of manuscript. All authors read and approved the final tion of thermostable xylanases by Thermomyces lanuginosus and Ther- manuscript moascus aurantiacus grown on lignocelluloses. Enzyme Microb Technol 16:298–302. https ://doi.org/10.1016/0141-0229(94)90170 -8 Funding Amore A, Parameswaran B, Kumar R et al (2015) Application of a new xylanase The authors thank Department of Biotechnology, Government of India (Grant activity from Bacillus amyloliquefaciens XR44A in brewer’s spent grain Nos. BT/304/NE/TBP/2012 and BT/PR7333/PBD/26/373/2012). saccharification. J Chem Technol Biotechnol 90:573–581. https ://doi. org/10.1002/jctb.4589 Availability of data and materials Andrews SR, Taylor EJ, Pell G et al (2004) The use of forced protein evolution to Not applicable. investigate and improve stability of family 10 xylanases the production of Ca2 -independent stable xylanases. J Biol Chem 279:54369–54379 Ethics approval and consent to participate Ang SK, Ariyani LP et al (2013) Production of cellulases and xylanase by Asper- Not applicable. gillus fumigatus SK1 using untreated oil palm trunk through solid state fermentation. Process Biochem 48:1293–1302. https ://doi.org/10.1016/j. Consent for publicationprocb io.2013.06.019 Not applicable. Anthony P, Harish BS, Jampala P et al (2016) Statistical optimization, purifica- tion and applications of xylanase produced from mixed bacteria in Competing interests a solid liquid fermentation using Prosopis juliflora. Biocatal Agric The authors declare that they have no competing interests. Biotechnol 8:213–220 Azeri C, Tamer UA, Oskay M (2010) Thermoactive cellulase-free xylanase pro- Received: 18 July 2019 Accepted: 9 October 2019 duction from alkaliphilic Bacillus strains using various agro-residues and their potential in biobleaching of kraft pulp. 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