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Detoxification approaches of mycotoxins: by microorganisms, biofilms and enzymes

Detoxification approaches of mycotoxins: by microorganisms, biofilms and enzymes Mycotoxins are generally found in food, feed, dairy products, and beverages, subsequently presenting serious human and animal health problems. Not surprisingly, mycotoxin contamination has been a worldwide concern for many research studies. In this regard, many biological, chemical, and physical approaches were investigated to reduce and/ or remove contamination from food and feed products. Biological detoxification processes seem to be the most promising approaches for mycotoxins removal from food. The current review details the newest progress in biologi- cal detoxification (adsorption and metabolization) through microorganisms, their biofilms, and enzymatic degrada- tion, finally describing the detoxification mechanism of many mycotoxins by some microorganisms. This review also reports the possible usage of microorganisms as mycotoxins’ binders in various food commodities, which may help produce mycotoxins-free food and feed. Keywords: Detoxification, Mycotoxins, Microorganisms, Biofilm, Enzymatic degradation both humans and animals (Milićević et al. 2010; Cwalina- Introduction Ambroziak et al. 2017; Vargas et al. 2001; El Khoury and Mycotoxins are secondary toxic metabolites produced Atoui 2010; El Khoury et  al. 2011; Battilani et  al. 2016; mainly by some fungal species belonging to Aspergillus, Nahle et  al. 2020). Exposure to mycotoxins can occur Penicillium, and Fusarium genera (Greeff-Laubscher directly through the ingestion of contaminated food or et al. 2020). Mycotoxin production can occur either in the indirectly through bi-products of animals consuming pre-harvest stage or in the post-harvest and storage ones contaminated feed (Bullerman 1979). Each year myco- under favorable environmental conditions (Waliyar et al. toxin contamination causes severe losses worldwide at 2014). The most important conditions for fungal growth the level of humans, animals, agriculture, and industries and mycotoxin production are temperature and water (WHO 2016). Therefore, with such negative impacts, activity (Peraica et  al. 1999; Darwish et  al. 2014). More regulatory guidelines and limits for mycotoxin in foods than 400 different types of mycotoxins have been iden - and feed have been set by various countries to control tified with different levels of toxicity. Among all myco - contamination levels in the food markets. Moreover, toxins, aflatoxins (AFs), Ochratoxin A (OTA), patulin researchers have been working on establishing several (PAT), Zearalenone (ZEN), and Trichothecenes (TCT) other ways to control mycotoxins in food and feed. have received particular attention due to their severe Over the last years, physical, chemical, and biological health outcomes on both humans and animals that can detoxification processes have been developed and they range from acute to severe and chronic intoxications in intended to mitigate mycotoxins in food and feed through destroying, modifying, or adsorbing them (El-Nezami *Correspondence: aatoui@ul.edu.lb et  al. 1998; Karlovsky 1999; Scudamore 2005; Varga and Research Laboratory of Microbiology (RLM), Department of Life Tóth 2005; Leong et al. 2006; Shetty et al. 2007; Dao and and Earth Sciences, Faculty of Sciences I, Lebanese University, Hadat Campus, Beirut, Lebanon Dantigny 2011; El Khoury et  al. 2011; Karlovsky et  al. Full list of author information is available at the end of the article 2016; Assaf et  al. 2017; Muhialdin et  al. 2020). Mainly, © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visithttp:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 2 of 14 Physical methods comprise quick-drying, UV treatment, and potential degradation (Muhialdin et  al. 2020). The and floating which help reduce mycotoxins during post- microorganisms implicated in biological degradation harvest applications (Brandt and Klebaum 2009). More- should follow certain standards such as being safe, non- over, various organic, inorganic, or mineral mycotoxins’ pathogenic, possess mycotoxins degrading ability, pertain binders were studied for their ability to adsorb myco- activity during packing, do not form improper odors or toxins, (Fandohan et  al. 2005; Scudamore et  al. 2007; taste, and preserve the nutrient value of food (Varga and Khatibi et  al. 2014; Assaf et  al. 2017; Assaf et  al. 2018a, Tóth 2005). The benefits of the biological detoxification b, c; Assaf et al. 2019a; Assaf et al. 2019b). Although they process include its easiness, cost-effectiveness, applica - have been shown to reduce their bioavailability, however, bility over broad range of target mycotoxins, efficacy in they still cannot adsorb them completely. Moreover, their a wide range of fluid and foodstuffs, and its insignificant application as a detoxification method showed many effects against nutrients naturally found in food (Varga drawbacks such as limited implementation, insignificant and Tóth 2005; Muhialdin et al. 2020). efficacy, and low potential as a detoxification approach when applied to foods (Assaf et  al. 2019a). On the other Biological and organic binders hand, chemical processes, including ammoniation, ozo- Various biological assays using either biological binders nation, peroxidation, and others have been reported to (bacteria, biofilm, and yeast) or organic binders (chitin, destroy mycotoxins from foodstuffs (Norred et  al. 1991) shrimp shells) have been established to remove different while however, failing to fulfill the criteria of a successful mycotoxins from laboratory liquid media or commer- detoxification process due to the negative outcomes on cial beverages by adsorption mechanism (Hatab et  al. food nutritional value, efficacy, and safety. Additionally, 2012; Taheur et  al. 2017; Chlebicz and Śliżewska 2020). chemical methods are expensive and require complicated Briefly, adsorption is an interaction mechanism between specifications to accomplish the detoxification process a special structure on the surface of the binder and the (Karlovsky 1999; Li et  al. 2020). Thus, both physical and mycotoxin through non-covalent bonds such as Van der chemical methods are not considered as adequately effec - Waals interactions, that reduces the bioavailability of the tive in removing mycotoxins from food and feed. mycotoxin found in the intended food commodity. On Therefore, this issue has directed researchers to find the other hand, biosorption is the use of biological bind- alternative mycotoxin detoxification methods that would ers for the detoxification process (Kolosova and Stroka rather be highly efficient and safe. Recently, many stud - 2011). The biosorption pathway is quick and direct in ies have focused on the usage of some microorganisms sequestering mycotoxins as compared to the biodeg- including lactic acid bacteria (LAB), yeast, and fungi to radation pathway. However, the toxins might be easily remove mycotoxins from food (Abrunhosa et  al. 2002; released back and this depends on the stability of the Assaf et  al. 2018a, b, c; Assaf et  al. 2019a; El-Nezami complex formed between the bacterial surface and the et  al. 2004a, b, El-Nezami et  al. 1998). In addition, the toxins (Solis-Cruz et al. 2019). use of microorganisms’ enzymes and their metabolites also showed efficiency in the mycotoxin degradation Bacteria processes (Karlovsky 1999; Li et al. 2020). The biological Many studies have reported that bacteria are useful bio- methods used in the removal and degradation of myco- logical agents for mycotoxin detoxification. Bacteria toxins are attractive and environmentally friendly and can remove mycotoxin by biosorption or biodegrada- therefore may offer better substitutes to the chemical tion mechanisms. A summary of the literature reporting and physical methods (Assaf et al. 2018a, b, c; Assaf et al. bacterial strains for mycotoxins detoxification in various 2019a). media is presented in Table  1. The removal percentage This review aims to discuss the biological decontami - of many mycotoxins involving various bacterial strains nation of mycotoxins and to review the mechanisms of reached a high efficiency of up to 94%. detoxification by yeasts and bacteria, in addition to bac - It was demonstrated that the use of Generally Recog- terial biofilms and their enzymes. Moreover, this review nized as Safe (GRAS) probiotic bacteria such as LAB is presents the contribution of biological detoxification very promising in mycotoxins detoxification (Abdelmo - methods to food safety and consumers’ health. tilib et al. 2018; El-Nezami et al. 1998; Fuchs et al. 2008; Assaf et  al. 2019a; Assaf et  al. 2018a, b, c; Ben Taheur Biological detoxification of mycotoxins using et  al. 2019; Wang et  al. 2018a, b). Haskard et  al. (2001) microorganisms revealed that several LAB has been established to detox- The biological detoxification of mycotoxins is defined ify AFB which is the most potent human carcinogen. as the usage of microorganisms, as well as their micro- Haskard and his team have assessed the ability of five bial enzymes and metabolites for mycotoxins binding Lactobacillus strains: L. rhamnosus GG, L. rhamnosus Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 3 of 14 Table 1 Mycotoxins removal percentage of different bacterial strains Strain Mycotoxins Sample Removal (%) References Lactobacillus acidophilus VM20 OTA Liquid medium 97 (Fuchs et al. 2008) Lactobacillus bulgaricus OTA PBS 94 ( Varga et al. 2005) Lactobacillus plantarum PAT Apple juice 91.2 (Zoghi et al. 2017) Lactobacillus rhamnosus LC705 AFB PBS 87.8 (Haskard et al. 2001) Lactobacillus rhamnosus GG AFB PBS 84.1 (Haskard et al. 2001) Lactobacillus kefiri KFLM3 OTA Milk 81 ( Taheur et al. 2017) Lactobacillus rhamnosus 6224 PAT Apple juice 80.4 (Hatab et al. 2012) Bifidobacterium animalis VM 13 PAT Liquid medium 80 (Fuchs et al. 2008) Lactobacillus rhamnosus 1088 AFB PBS 79 (Chlebicz and Śliżewska 2020) Lactobacillus rhamnosus GG ZEN PBS 70 (El-Nezami et al. 2002) Enterococcus faecium 21,605 PAT Apple juice 64.5 (Hatab et al. 2012) Lactobacillus rhamnosus GG AFM PBS 63.1 (Assaf et al. 2017) Lactobacillus rhamnosus GG biofilm AFM Milk 60.7 (Assaf et al. 2019a) Actinobacteria AT8 OTA PBS 52.6 (El Khoury et al. 2017) Lactobacillus plantarum 13 M5 PAT Apple juice 43.8 ( Wei et al. 2020) Lactobacillus plantarum VM 37 OTA Liquid medium 43 (Fuchs et al. 2008) Lactobacillus plantarum VM 37 PAT Liquid medium 39 (Fuchs et al. 2008) LC705, L. acidophilus, L. gasseri, and L. casei to remove Mycotoxins binding in several studies was reported AFB from liquid media and have demonstrated that the to be rapid, and the binding percentages were generally probiotic strains L. rhamnosus GG and L. rhamnosus affected by many factors such as incubation time, type of LC705 were highly effective in detoxifying of up to 80% bacteria, bacterial concentration, pH, type of medium, AFB (Haskard et al. 2001). Additionally, El-Nezami et al. and temperature (El-Nezami et  al. 2004a). The use of (2002) have shown that L. rhamnosus GG was able to bacterial adsorbents in beverages presents several advan- remove up to 70% of ZEN from liquid media. Fuchs et al. tages over chemical and physical detoxification methods. (2008) showed that Bifidobacterium animalis strain VM The bacterial detoxification assay is considered more 12 was able to remove approximately 80% of PAT and L. effective and highly specific, especially since the binding acidophilus strain (VM 20) reduced the OTA levels by affinity of mycotoxins varies not only among different more than 90% among all tested strains. species but also among different strains within the same Other strains of bacteria have been investigated for species. Furthermore, the use of several probiotic bacte- their binding capability to mycotoxins. El Khoury et  al. ria has made the bacterial detoxification process safer. (2017) have investigated the ability of actinobacteria, which are found in soil habitat and comprise the larg- Yeasts est bacterial genera “Streptomyces”, to bind and detoxify Studies showed that probiotic yeasts or products con- OTA. El Khoury et al. (2017) have established that seven taining yeast cell walls can remove mycotoxins from different strains of actinobacteria were able to bind OTA beverages (Pizzolitto et  al. 2012). A summary of the lit- to different extents. Among the tested strains, AT8 strain erature in which yeast strains were used for mycotox- was remarkably able to detoxify OTA to up to 52.61%. ins detoxification is presented in Table  2. Generally, it Also, Verheecke et al. (2014) have found that the mutual is well established that S. cerevisiae is extensively used interaction between Streptomyces spp. (27 strains) and in biotechnology processes such as baking and distill- Aspergillus flavus (NRRL 62477) can reduce the level of ing industries. Some studies shown that S. cerevisiae AFB and AFB in vitro to up to 73%. In 2018, Wang et al. can remove OTA from microbiological media and other 1 2 (2018a, b) have shown that Lysinibacillus sp. strain, iso- beverages (Piotrowska and Masek 2015). Other studies lated from chicken large intestine digesta, demonstrated have demonstrated that S. cerevisiae is most effective in high ability in removing ZEN. Additionally, Taheur et al. AFB binding (Corassin et al. 2013). Corassin et al. (2013) (2017) have proved that Lactobacillus kefiri, Kazach- have demonstrated that heat-killed S. cerevisiae cells have stania servazzii, and Acetobacter syzygii were able to the potential to reduce AFM levels in milk. Other yeast remove up to 100% of AFB . strains such as Kluyveromyces Lactis and Kazachstania 1 Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 4 of 14 Table 2 Mycotoxins removal percentage of different yeast strains Strain Mycotoxins Sample Removal (%) References S. cerevisiae AFM UHT skim milk 90.3 (Corassin et al. 2013) S. cerevisiae RC008 OTA YPD broth 82.3 (Armando et al. 2012) S. cerevisiae AFM PBS 78.7 (Abdelmotilib et al. 2018) S. cerevisiae YS3 PAT Apple juice 72.6 (Yue et al. 2011) Kluyveromyces Lactis AFM PBS 69.1 (Abdelmotilib et al. 2018) Kazachstania servazzii KFGY7 OTA Milk 62 ( Taheur et al. 2017) S. cerevisiae 0068 AFB PBS 46.7 (Chlebicz and Śliżewska 2020) servazzii KFGY7 also showed removal ability of mycotox- microorganisms is a rapid process, which forms a revers- ins from milk reaching to up to 69.14%. ible complex between the toxin and the bacterial surface without altering the mycotoxins’ structure (Bueno et  al. Chitin and shrimp shells 2007). Shetty and Jespersen’s investigations revealed that Both polysaccharides and peptidoglycans are found in the detoxification process is related to a physical union the cell wall of different microorganisms and have been between the mycotoxins and the bacterial cell compo- shown to be involved in mycotoxin binding (Kim et  al. nents, instead of covalent binding or biodegradation by 2017). The amino sugar N-acetyl-D-glucosamine (Glc - bacterial metabolism (Shetty and Jespersen 2006). Yian- NAc) is the key component of the cell wall of microor- nikouris et  al. (2006) reported that hydrogen bonds and ganisms including fungi, bacteria, and yeast (Chen et  al. Van der Waals interactions may be implicated in this 2010), and this has been mainly responsible for the binding mechanism. On the other hand, according to detoxification of mycotoxins (Assaf et  al. 2018a , b, c). Hernandez-Mendoza et  al. (2009), the differences in This sugar is also found in the exoskeleton of crustaceans the mycotoxins’ binding ability of various Lactobacillus in the form of a polymer known as “chitin”, specifically in strains could be explained by the differences in the cell shrimp shells (Xu et al. 2008; Iqbal et al. 2017) that con- wall components specifically teichoic acid and pepti - tain primarily 30–40% of chitin (Venugopal 2016). In that doglycan contents. Different structures in the cell wall of sense, attention has been given to chitinous polymers microorganisms are responsible for the mycotoxin bind- and shrimp shells and their ability to remove mycotox- ing capacity. Cell walls comprise carbohydrates (pep- ins. Assaf et al. (2018a, b, c) have evaluated the ability of tidoglycan, mannose, and glucan), proteins, and lipids, chitin (as a natural biopolymer) and ground shrimp shells which may offer different binding sites (Wang et  al. (which contain 30–40% of chitin) to detoxify A FM . They 2019a, b). However, there are arguments among different showed that chitin and shrimp shells were able to bind researches on the specific cell wall components impli - AFM in milk at varied binding percentages in the range cated in the binding processes, such as glucogalactans of 14.29 and 94.74%. Yearly, up to 8 million tons of crab, and β-glucans (Taheur et  al. 2017), mannoproteins shrimp, and lobster shells are wasted worldwide, (Yan (Caridi et  al. 2012), β- glucans and mannans (Pereyra and Chen 2015) thus, valorisation of these wastes, to be et al. 2015). Therefore, in the interaction of bacterial cells used as potential biosorbents in mycotoxin detoxification and mycotoxins, it appears that various binding mecha- would contribute to decreasing food waste and eliminat- nisms may be implicated involving non-covalent bond- ing toxic effects on humans. They would also be of great ing, hydrophobic interactions, ionic interactions, or interest as an added benefit to the food industry. hydrogen bonds, (Huwig et al. 2001; Ringot et al. 2007). The cell wall portion of S. cerevisiae is mostly com - Mechanisms of action involved through microbial binding posed of polysaccharides with an inner layer of β-D- To date, there are two theories by which LAB elimi- glucans chains, which constitute 50 to 60% of the wall’s nates toxins: one through physical adsorption and the dry weight (Jouany et  al. 2005). Jouany et  al. (2005) other through biodegradation of mycotoxins. Research- have shown that β-D-glucans are the components ers have conducted several detoxification experiments mainly responsible for the complexation of ZEN. Also, to test which theory is more adequate. Experiments they showed that the chemical interaction is more of an with thermally inactivated bacteria provoked higher adsorption type than binding, where both weak hydro- detoxification of mycotoxins as compared to activated gen bonds and Van der Waals interactions are involved cells. Studies showed that the binding of mycotoxins by in this adsorption. Moreover, it has been demonstrated Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 5 of 14 Detoxification approaches of mycotoxins by biofilms that the binding process of OTA to the surface of living Bacteria exist in nature under two forms: either as freely or dead yeast cells, is achieved, in general, by adsorp- swimming planktonic bacteria, or as sessile in attached tion mechanisms (Bejaoul et  al. 2004). These research - colonies of microorganisms forming a biofilm. Thus, ers have concluded that the yeast cell wall and its the biofilm may be considered as “a three-dimensional charge are involved in the adsorption process (Bejaoul structure of sessile microorganisms that are irreversibly et  al. 2004). These observations were similar to those attached to biotic or abiotic surfaces, embedded in self- of Piotrowska (2014) who found that bacteria, with formed extracellular polymeric substances (EPS) (Lewan- partially removed cell walls, had less ability to bind dowski and Boltz, 2010). OTA, as compared to the bacteria with intact cell walls In the last decades, biofilm formation has been impli - (Piotrowska 2014), highlighting, therefore, the impor- cated in many industrial and domestic domains (Roger tance of the cell wall in the adsorption mechanisms et al. 2008). Salas-Jara et al. (2016) have studied the abil- (Piotrowska 2014). ity of some strains of LAB to form a biofilm and Lebeer The properties of the bacterial cell surface play a et  al. (2007) have shown the ability of L. rhamnosus GG vital role in the binding mechanism. In another study, to form biofilm on polystyrene support. Recently, a new involving Escherichia coli, a Gram-negative bacterium, method was developed for the detoxification of milk it was established that it was incapable of removing from AFM by using L. rhamnosus GG biofilm (Assaf mycotoxins due to its moderately hydrophilic nature et  al. 2019a). The biofilm was formed on polystyrene and its present surface components (lipopolysaccha- petri plates and in polyethylene tubes. The detoxification rides) (Pierides et  al. 2000). On the other hand, LAB process was carried out using the biofilm formed on day bacteria having hydrophobic sites on their cell surface 3, which is considered a highly attached biofilm and an were confirmed to have the ability to bind OTA (El- efficient binding agent. The percentages of bound AFM Nezami et  al. 1998). Assaf et  al. (2019a) hypothesized by L. rhamnosus GG biofilm reached to up to 60.7%. that the biofilm matrix may be involved in AFM bind- Moreover, the quality of milk after A FM detoxification ing rather than the bacterial cells themselves. Addi- had no significant changes in the protein content, but tionally, this study observed that washing the biofilm some changes in fat and total dry matter contents ratio. had released some fraction of the weakly bound AFM . Additionally, Assaf et  al. (2019a) have studied the stabil- This confirms that binding is reversible due to the dis- ity of the AFM -biofilm complex using different AFM ruption of some electrostatic bonds as hydrogen bonds 1 1 concentrations. The study has shown that the binding and Van der Waals interactions (Hernandez-Mendoza was reversible and a portion of the bound A FM was et al. 2009). released after successive washings. To date, this tech- Moreover, higher mycotoxins’ elimination was shown nique is a modern technique that relies on the removal of by inactivated bacterial cells. For example, Haskard mycotoxins by a biofilm, making it of great challenge and et  al. (2001) found that high temperature leads to pro- appeal, especially to those that are interested in remov- tein denaturation in the bacterial cell wall, and this ing mycotoxins from foods. However, the use of biofilms results in the generation of pores, that facilitate further as a technique of detoxification of mycotoxins is still in aflatoxins’ adsorption and mycotoxins elimination. its early stages and additional studies that might be of a Additionally, the same authors suggested that protein potential usefulness to food industries should be con- denaturation might increase the hydrophobic nature ducted. Hence, on a general note, using biofilms as bio - of the surface or form Maillard reaction products and logical adsorbents for mycotoxins may be considered as such alterations allow aflatoxins to bind to the bacterial a solid base for the progress of biological detoxification cell wall and plasmatic membrane components, which methods. were masked when the cell wall was intact (Haskard et  al. 2001). Chlebicz and Śliżewska (2020) recently Detoxification approaches of mycotoxins by microbial have shown that treatment of yeasts by heat and acid- enzymes ity improved significantly OTA detoxification by up to Enzymatic detoxification is one of the most promis - 75% from liquid medium compared to untreated cells. ing methods of mycotoxins control, especially that it is Expecting that both polysaccharides and peptidogly- devoid of some significant disadvantages that chemical cans are affected by heat and acid treatments, these methods employ such as chemical contamination of raw researchers postulated that acidic treatments could materials, nutrient loss, time-consuming and expensive disturb polysaccharides, by releasing monomers that (Wang et al. 2019a, b). A wide range of microorganisms are broken down into aldehydes, which could lead to including bacteria, molds, and yeasts are involved in more adsorption sites than viable cells (Chlebicz and the enzymatic detoxification of mycotoxins (Hathout Śliżewska 2020). Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 6 of 14 and Aly 2014). Generally, microbial enzymes are able to The mycotoxins detoxification efficacy of different metabolize, destroy or inactivate mycotoxins into less enzymes produced as part of the yeasts/fungi metabolic or nontoxic metabolites (Lyagin and Efremenko 2019). activity are summarized in Table 3. Degradation is a process by which most of the micro- In one of the first studies to be conducted on microbial organisms use during their life activities to degrade enzymes, manganese peroxidase can serve as a good can- certain substances converting them into less or even didate for detoxifying various types of mycotoxins (Wang non-toxic products. During the degradation process, et  al. 2011). This peroxidase, purified from different lig - the vital active molecules secreted by microorganisms nocellulose-degrading fungi such as Irpex lacteus, Phan- are enzymes (Guan et al. 2021). erochaete chrysosporium, Ceriporiopsis subvermispora, Most of the scientific studies to date are dedicated to and Nematoloma frowardii, can degrade AFB , ZEN, and enzymatic degradation for detoxifying the most notable other mycotoxins (Tang et al. 2013). Loi et al. (2018) have mycotoxins, including AF, OTA, ZEN, TCT, and PAT described the ability of laccase purified from Pleurotus (Tang et  al. 2013; Loi et  al. 2018; Zhang et  al. 2020). eryngii to simultaneously degrade A FB and ZEN by 86% Several microbial enzymes from bacteria, yeast, and and 100% respectively. fungi that are capable of performing various modifica - Interestingly, Bacillus pumilus ES-21 was able to tions or transformations of mycotoxins have been iso- degrade 95.7% of ZEN into 1-(3,5-dihydroxyphenyl)- lated and investigated (Ben Taheur et al. 2019). 6-hydroxy-l-undecen-l0-one (Wang et  al. 2017). Overall, Examples of microbial enzymes, reported in the lit- three kinds of enzymes have been identified to degrade erature, involved in mycotoxins degradation are pre- ZEN: Lactonase (Bi et al. 2018; Wang et al. 2018a, b), per- sented in Table  3. Studies have shown that some oxidase (Tang et  al. 2013), and laccase (Loi et  al. 2018). enzymes from yeasts have important characteristics Lactonase ZHD101 was mostly proposed for its high that enable them to transform toxins into less toxic efficiency in ZEN degrading ability, found in S. cerevisiae ones (Schatzmayr et  al. 2006; Halász et  al. 2009). A (Takahashi-Ando et  al. 2002) and L. reuteri (Yang et  al. number of enzymes belonging to Aspergillus species are 2017). Even though lactonase has high degrading abil- found to be involved in aflatoxin degradation. Further - ity, however, it is not highly thermostable which restricts more, Aspergillus niger, an isolate from feed samples, its applications (Zhang et al. 2020). Recently, Wang et al. was shown to biodegrade AFB (Zhang et  al. 2014). (2018a, b) identified a lactonohydrolase enzyme, Zhd518, Other fungal strains that may contribute to the detoxi- which exhibited high degrading activity against ZEN. The fication of aflatoxins, by secreting oxidative enzymes same authors reported that Zhd518 could be an excel- such as laccase and manganese peroxidase have been lent candidate for ZEN detoxifying due to its high spe- reported (Alberts et  al. 2009). Interestingly, manga- cific activity against ZEN and its derivatives (Wang et al. nese peroxidase extracted from Phanerochaete sordida 2018a, b). Recently, Zhang et  al. (2020) have identified was responsible for eliminating 86% of A FB in  vitro, an effective ZEN-degrading lactonase from Gliocladium increasing to 100% with successive additions of the roseum, named ZENG for the first time (Zhang et  al. enzyme (Wang et  al. 2011). Moreover, laccase enzyme 2020). This recombinant enzyme has great activity and purified from Trametes versicolor was able to remove stability at a pH of 7.0., characterized by its great detoxi- 67% of AFB (Zeinvand-Lorestania et al. 2015). fication ability of ZEN and its derivatives, α-zearalenol Recently, Zhang et al. (2018) showed that the intracel- (α-ZOL), and α-zearalanol (α-ZAL) (Zhang et al. 2020). lular enzymes of Y. lipolytica Y-2 were able to degrade OTA more rapidly than its viable cells (Zhang et  al. Mechanisms of action involved in the enzymatic 2018). Also, Chang et al. (2015) have reported that car- transformation of mycotoxins boxypeptidase, an enzyme purified from B. amylolique - Many biochemical transformation reactions of myco- faciens ASAG1 was capable of reducing OTA by 72%. toxins by microorganisms and their enzymes have been Additionally, the enzymatic extracts from Rhodoc- described such as acetylation, glucosylation, ring cleav- occus erythropolis, N. corynebacterioides DSM 20151, age, hydrolysis, sulfation, deamination, and decarboxy- and M. fluoranthenivorans sp. nov. DSM 44556 T have lation (Li et  al. 2020). Some of the biotransformation revealed more than 90% degradation capability of reactions of mycotoxins by some microbial enzymes are AFB (Hackbart et al. 2014). Recently, Shu et al. (2018) shown in Table 4. established that heat-treated supernatant from Bacil- lus velezensis DY3108 was able to degrade 94.7% of Application of biological detoxification processes AFB into less toxic metabolites. Recently, it was found in the food industry that Bacillus pumilus was able to degrade 88% of A FB Many microorganisms have been proposed for use as (Sangi et al. 2018). detoxifying agents in food and feed, but only few have Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 7 of 14 Table 3 Examples of some types of biotransformation reactions and the involved microorganisms or enzymes Type of Bio- Hydrogenation Hydroxylation Sulfation Reduction of the ketonic carbonyl Transformation group Reaction Substrate Product Microorganism or Penicillium raistrickii Phenylobacterium Sphaerodes mycoparasitica Rhizopus sp., Aspergillus sp Enzyme References (Wu et al. 2009) (Wegst and Lingens 1983) (Kim and Vujanovic 2017) (Brodehl et al. 2014) Type of Bio- Hydrolysis Oxido-Reduction Reduction of Carbonyl group Transformation Reaction Substrate Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 8 of 14 Table 3 (continued) Type of Bio- Hydrogenation Hydroxylation Sulfation Reduction of the ketonic carbonyl Transformation group Reaction Product Microorganism or Aspergillus niger/ Lipase Bacillus pumilus ES-21 /purified lactonase Lactobacillus plantarum Aspergillus niger, Eurotium herbariorum, Enzyme Rhizopus sp. References (Stander et al. 2000) (Xu et al. 2016; Wang et al. 2017) (Soukup et al. 2016) (Nakazato et al. 1991) Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 9 of 14 Table 4 Examples of enzymes and their microorganism origin that are involved in the degradation of mycotoxins Microbial Origin Name of enzyme Mycotoxins Degradation (%) References Or Type of enzyme Aspergillus niger MUM 03.58 Carboxypeptidase OTA 99 (Abrunhosa et al. 2006) Bacillus amyloliquefaciens ASAG1 Carboxypeptidase OTA 72 (Chang et al. 2015) Aspergillus tubingensis M036 – OTA 97.5 (Cho et al. 2016) Aspergillus tubingensis M074 – OTA 91.3 (Cho et al. 2016) Aspergillus niger Ochratoxinase OTA ND (Dobritzsch et al. 2014) Yarrowia lipolytica Y-2 Carboxypeptidases OTA ND (Zhang et al. 2018) Phanerochaete sordida Manganese peroxidase AFB 86 ( Wang et al. 2011) Trametes versicolor Laccase AFB 67 (Zeinvand-Lorestania et al. 2015) Pleurotus eryngii Laccase AFB 86 (Loi et al. 2018) Pleurotus eryngii Laccase ZEN 100 (Loi et al. 2018) Escherichia coli Lactonohydrolase Zhd518 ZEN ND ( Wang et al. 2018b) lignocellulose-degrading fungi Manganese Peroxidase ZEN 34.0 ( Tang et al. 2013) lignocellulose-degrading fungi Manganese Peroxidase AFB 84.9 ( Tang et al. 2013) Rhodococcus erythropolis – AFB 90 (Hackbart et al. 2014) Bacillus velezensis DY3108 – AFB 94.7 (Alberts et al. 2009) Bacillus pumilus – AFB 88 (Alberts et al. 2009) Bacillus pumilus ES-21 – ZEN 95.7 ( Wang et al. 2017) Gliocladium roseum ZENG ZEN 60 (Zhang et al. 2020) Aspergillus niger – AFB 23.6 (Zhang et al. 2014) Peniophora sp. SCC0152 – AFB 40.45 (Alberts et al. 2009) been further investigated for uses in the food indus- samples where the highest detoxification percentage try. Many factors should be considered while selecting reached was 81.3% without altering the physicochemical a binder for mycotoxins, particularly in the food sector, properties of milk. Further optimization of the bio-filters including non-pathogenicity, specificity, effective seques - may subsequently lead to different practical detoxifica - tering and the absence of adverse effects. tion applications of various mycotoxins from dairy prod- Assaf et  al. (2018a, b, c) have proposed a novel ucts and beverages. machine that may be employed in the detoxification In a previous study, Hatab et al. (2012) showed that L. of mycotoxin from liquid beverages. This machine rhamnosus 6224 and Enterococcus faecium 21,605 were has probiotic LAB biofilms fixed to a customized car - able to remove 80.4 and 64.5% of patulin (PAT) from tridge; accordingly, it allows liquid food to pass through apple juice, respectively. These researchers have proved these adsorbents which results in detoxified liquid. The that LAB could be used as a novel and promising adsor- prototype of the invested detoxifying machine is pre- bent to bind PAT without altering the quality of the juice. sented in Fig.  1. Many aspects, such as the flow rate of Yue et al. (2011) have shown that inactivated S. cerevi- the pump, the number of cartridges utilized, the kind siae YS3 powder was able to remove up to 72.61% of PAT of biological adsorbents are proposed to be explored from apple juice, and additionally, there was no negative throughout the development of this machine prototype. impact on the quality of apple juice, based on the quality This machine has the potential to be a promising appli - parameters measured, such as degrees Brix, total sugar, cation in liquid food purification, particularly because titratable acidity, color value, and clarity. This study sug - the creation of biofilms is cost-effective, however, it is gests that the inactivated S. cerevisiae YS3 powder could also very important to assess the effect of this treat - be a hopeful binder of PAT in apple juice, especially since ment on the organoleptic characteristics of the bever- yeast has low cost, high biomass properties, and can be ages after detoxification process. simply separated from apple juice (Yue et al. 2011). Lately, Foroughi et al. (2018) have suggested a method Although many articles on mycotoxin elimination to detoxify AFM -contaminated milk by immobilizing by adsorption and transformation have been pub- yeast such as S. cerevisiae on perlite support. The results lished, their applicability in the food industry has been revealed a high significant removal of AFM from milk restricted. This might be attributed to a lack of knowledge 1 Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 10 of 14 Fig. 1 Prototype machine for detoxification of mycotoxins from beverages using biological adsorbents regarding transformation processes, the toxicity of trans- identifying the transformed products, and (ii) performing formation products, and the influence of transformation toxicity assays on the resultant intermediate metabolites reactions on the nutritional content of food and feed. and products. Meanwhile, because the enzyme’s genetic Degraded products have not been recognized in certain sequence is known, molecular engineers might improve circumstances and so cannot be employed in industrial the enzyme’s selectivity and catalytic performance by operations. making changes to the active region. All of these per- Recently, Zhang et  al. (2020) have identified a potent ceptions should be taken into account in order to aid in enzyme, ZENG, that is efficient in detoxifying up to 60% the mitigation of mycotoxins. Biological degradation of of ZEN and its toxic derivatives. However, most enzymes mycotoxins is a promising method that can be further do not meet the requirements of industrial applications developed by focusing on the isolation of specific micro - due to their low ability to withstand high temperatures organisms, optimizing their growth, and creating condi- (Atalah et  al. 2019). So thermostability is an important tions that favor massive production of enzymes. characteristic of industrial enzymes and to meet the industrial demands, efforts should also seek to provide Conclusion highly thermostable enzymes, which can reduce the cost Mycotoxins have received much attention due to their of production, develop its efficiency, and help in lowering severe impact on human and animal health. Their microbial contamination in industrial approaches. detoxification has been always the goal of research. Although, an enzymatic catalysis is a promising While biological detoxification of mycotoxins has been approach that can be used to detoxify mycotoxins (Ben widely studied, little is still known about the potential Taheur et  al. 2019). However, not all mycotoxins’ modi- applications in the food, feed, and beverages industries. fications and transformations can lead to detoxification So practically, scientists should focus on the potential products. For example, Hahn et  al. (2015) showed that use of microorganisms in the detoxification of myco - the α- and/or β-ZOL, the reduced products of ZEN, have toxin mixtures from food and beverages. In addition, it similar estrogenic activity compared to ZEN. Karabulut is of utmost importance to analyze the physicochemi- et  al. (2014) deduced that aflatoxicol, the reduced prod - cal profile, sensory properties, and organoleptic char - uct of AFB , has a similar ability to form an exo-epoxide acteristics of the juices and food after detoxification of analog that binds to DNA. mycotoxins. Further, it is necessary to isolate and select Enzymatic detoxification, in our opinion, might be a suitable enzymes and microorganisms for efficient viable technique for the majority of mycotoxins if applied detoxification and to analyze the enzymatic properties properly. The efficacy of the biodegradation process can and their catalytic processes in food and beverages. be validated by using two criteria: (i) discovering and In brief, what makes a good binder is its adsorption Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 11 of 14 Received: 12 December 2021 Accepted: 23 March 2022 capacity, specificity, safety, and stability. Therefore, after the future development of these promising approaches, enzymes and microorganisms can be used as food and feed additives or as detoxifying agents during food pro- References cessing, while preserving the nutritional and organo- Abrunhosa L, Serra R, Venâncio A (2002) Biodegradation of ochratoxin A by leptic quality of food commodities and beverages. fungi isolated from grapes. J Agric Food Chem 50:7493–7496. https:// doi. org/ 10. 1021/ jf025 747i Abdelmotilib NM, Of C, Applications T, Hamad G, Salem EG (2018) Aflatoxin M1 reduction in Milk by a novel combination of probiotic bacterial Abbreviations aflatoxin M1 reduction in Milk by a novel combination of probiotic AFs: Aflatoxins; OTA: Ochratoxin A; PAT: Patulin; ZEN: Zearalenone; TCT : Tri- bacterial and yeast strains. Nutr food Saf 8:83–99. https:// doi. org/ 10. chothecenes; LAB: Lactic Acid Bacteria; AFB : Aflatoxin B ; AFM : Aflatoxin M ; 1 1 1 1 9734/ ejnfs/ 2018/ 39486 PBS: Phosphate Buffer saline; AFB : Aflatoxin B ; GRAS: Generally Recognized 2 2 Abrunhosa L, Santos L, Venâncio A (2006) Degradation of Ochratoxin A by as Safe; EPS: Extracellular Polymeric Substances; α-ZOL: α-zearalenol; α-ZAL: proteases and by a crude enzyme of aspergillus Niger. Food Biotechnol α-zearalanol. 20:231–242 Alberts JF, Gelderblom WCA, Botha A, van Zyl WH (2009) Degradation of Acknowledgments aflatoxin B1 by fungal laccase enzymes. Int J Food Microbiol 135:47–52. This work was supported by the Conflicts of Interest research council and the https:// doi. org/ 10. 1016/j. ijfoo dmicro. 2009. 07. 022 research and analysis center (CAR) at the Faculty of Sciences in Saint-Joseph Armando MR, Pizzolitto RP, Dogi CA, Cristofolini A, Merkis C, Poloni V, Dalcero University (USJ ) and the Lebanese University through a grant 6341/4. AM, Cavaglieri LR (2012) Adsorption of ochratoxin A and zearalenone by potential probiotic Saccharomyces cerevisiae strains and its relation Authors’ contributions with cell wall thickness. J Appl Microbiol 113:256–264. https:// doi. org/ Sahar Nahle: Original draft preparation-Writing-Reviewing and Editing. Andre 10. 1111/j. 1365- 2672. 2012. 05331.x El Khoury: Reviewing-Editing. Ali Chokr: Reviewing-Editing. Nicolas Louka: Assaf JC, Atoui A, El Khoury A, Chokr A, Louka N (2017) A comparative study of Reviewing-Editing. Ioannis Savvaidis: Reviewing-Editing and Ali Atoui: Struc- procedures for binding of aflatoxin M1 to Lactobacillus rhamnosus GG. turing/Formulation, Reviewing-Editing. The author(s) read and approved the Brazilian J Microbiol 49:120–127. https:// doi. org/ 10. 1016/j. bjm. 2017. final manuscript. 05. 003 Assaf JC, El Khoury A, Atoui A, Chokr A (2018b) A novel process for detoxifica- Authors’ information tion of liquid foods from mycotoxins SN is a Ph.D. student between the Lebanese University and the Université Assaf JC, El Khoury A, Atoui A, Louka N, Chokr A (2018c) A novel technique for Saint-Joseph de Beyrouth. aflatoxin M1 detoxification using chitin or treated shrimp shells&nbsp;: AK is a Professor at the Faculté des Sciences, Université Saint-Joseph de in vitro effect of physical and kinetic parameters on the binding stabil- Beyrouth. ity. Appl Microbiol Biotechnol 102:6687–6697 IS is a Professor at the Department of Environmental Health Sciences, Univer- Assaf JC, Louka N, El Khoury A, Chokr AAA (2018a) A novel process for detoxifi- sity of Sharjah. cation of liquid foods from mycotoxins AC is a Professor at the Department of Life and Earth Sciences, Faculty of Sci- Assaf JC, El Khoury A, Chokr A, Louka N, Atoui A (2019a) A novel method for ences, Lebanese University. elimination of aflatoxin M1 in milk using Lactobacillus rhamnosus GG NL is a Professor at the Faculté des Sciences, Université Saint-Joseph de biofilm. Int J Dairy Technol 72:248–256. https:// doi. org/ 10. 1111/ 1471- Beyrouth. 0307. 12578 AA is a Professor at the Department of Life and Earth Sciences, Faculty of Sci- Assaf JC, Nahle S, Chokr A, Louka N, Atoui A, El Khoury A (2019b) Assorted ences, Lebanese University. methods for decontamination of aflatoxin M1 in Milk using microbial adsorbents. 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Detoxification approaches of mycotoxins: by microorganisms, biofilms and enzymes

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Abstract

Mycotoxins are generally found in food, feed, dairy products, and beverages, subsequently presenting serious human and animal health problems. Not surprisingly, mycotoxin contamination has been a worldwide concern for many research studies. In this regard, many biological, chemical, and physical approaches were investigated to reduce and/ or remove contamination from food and feed products. Biological detoxification processes seem to be the most promising approaches for mycotoxins removal from food. The current review details the newest progress in biologi- cal detoxification (adsorption and metabolization) through microorganisms, their biofilms, and enzymatic degrada- tion, finally describing the detoxification mechanism of many mycotoxins by some microorganisms. This review also reports the possible usage of microorganisms as mycotoxins’ binders in various food commodities, which may help produce mycotoxins-free food and feed. Keywords: Detoxification, Mycotoxins, Microorganisms, Biofilm, Enzymatic degradation both humans and animals (Milićević et al. 2010; Cwalina- Introduction Ambroziak et al. 2017; Vargas et al. 2001; El Khoury and Mycotoxins are secondary toxic metabolites produced Atoui 2010; El Khoury et  al. 2011; Battilani et  al. 2016; mainly by some fungal species belonging to Aspergillus, Nahle et  al. 2020). Exposure to mycotoxins can occur Penicillium, and Fusarium genera (Greeff-Laubscher directly through the ingestion of contaminated food or et al. 2020). Mycotoxin production can occur either in the indirectly through bi-products of animals consuming pre-harvest stage or in the post-harvest and storage ones contaminated feed (Bullerman 1979). Each year myco- under favorable environmental conditions (Waliyar et al. toxin contamination causes severe losses worldwide at 2014). The most important conditions for fungal growth the level of humans, animals, agriculture, and industries and mycotoxin production are temperature and water (WHO 2016). Therefore, with such negative impacts, activity (Peraica et  al. 1999; Darwish et  al. 2014). More regulatory guidelines and limits for mycotoxin in foods than 400 different types of mycotoxins have been iden - and feed have been set by various countries to control tified with different levels of toxicity. Among all myco - contamination levels in the food markets. Moreover, toxins, aflatoxins (AFs), Ochratoxin A (OTA), patulin researchers have been working on establishing several (PAT), Zearalenone (ZEN), and Trichothecenes (TCT) other ways to control mycotoxins in food and feed. have received particular attention due to their severe Over the last years, physical, chemical, and biological health outcomes on both humans and animals that can detoxification processes have been developed and they range from acute to severe and chronic intoxications in intended to mitigate mycotoxins in food and feed through destroying, modifying, or adsorbing them (El-Nezami *Correspondence: aatoui@ul.edu.lb et  al. 1998; Karlovsky 1999; Scudamore 2005; Varga and Research Laboratory of Microbiology (RLM), Department of Life Tóth 2005; Leong et al. 2006; Shetty et al. 2007; Dao and and Earth Sciences, Faculty of Sciences I, Lebanese University, Hadat Campus, Beirut, Lebanon Dantigny 2011; El Khoury et  al. 2011; Karlovsky et  al. Full list of author information is available at the end of the article 2016; Assaf et  al. 2017; Muhialdin et  al. 2020). Mainly, © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visithttp:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 2 of 14 Physical methods comprise quick-drying, UV treatment, and potential degradation (Muhialdin et  al. 2020). The and floating which help reduce mycotoxins during post- microorganisms implicated in biological degradation harvest applications (Brandt and Klebaum 2009). More- should follow certain standards such as being safe, non- over, various organic, inorganic, or mineral mycotoxins’ pathogenic, possess mycotoxins degrading ability, pertain binders were studied for their ability to adsorb myco- activity during packing, do not form improper odors or toxins, (Fandohan et  al. 2005; Scudamore et  al. 2007; taste, and preserve the nutrient value of food (Varga and Khatibi et  al. 2014; Assaf et  al. 2017; Assaf et  al. 2018a, Tóth 2005). The benefits of the biological detoxification b, c; Assaf et al. 2019a; Assaf et al. 2019b). Although they process include its easiness, cost-effectiveness, applica - have been shown to reduce their bioavailability, however, bility over broad range of target mycotoxins, efficacy in they still cannot adsorb them completely. Moreover, their a wide range of fluid and foodstuffs, and its insignificant application as a detoxification method showed many effects against nutrients naturally found in food (Varga drawbacks such as limited implementation, insignificant and Tóth 2005; Muhialdin et al. 2020). efficacy, and low potential as a detoxification approach when applied to foods (Assaf et  al. 2019a). On the other Biological and organic binders hand, chemical processes, including ammoniation, ozo- Various biological assays using either biological binders nation, peroxidation, and others have been reported to (bacteria, biofilm, and yeast) or organic binders (chitin, destroy mycotoxins from foodstuffs (Norred et  al. 1991) shrimp shells) have been established to remove different while however, failing to fulfill the criteria of a successful mycotoxins from laboratory liquid media or commer- detoxification process due to the negative outcomes on cial beverages by adsorption mechanism (Hatab et  al. food nutritional value, efficacy, and safety. Additionally, 2012; Taheur et  al. 2017; Chlebicz and Śliżewska 2020). chemical methods are expensive and require complicated Briefly, adsorption is an interaction mechanism between specifications to accomplish the detoxification process a special structure on the surface of the binder and the (Karlovsky 1999; Li et  al. 2020). Thus, both physical and mycotoxin through non-covalent bonds such as Van der chemical methods are not considered as adequately effec - Waals interactions, that reduces the bioavailability of the tive in removing mycotoxins from food and feed. mycotoxin found in the intended food commodity. On Therefore, this issue has directed researchers to find the other hand, biosorption is the use of biological bind- alternative mycotoxin detoxification methods that would ers for the detoxification process (Kolosova and Stroka rather be highly efficient and safe. Recently, many stud - 2011). The biosorption pathway is quick and direct in ies have focused on the usage of some microorganisms sequestering mycotoxins as compared to the biodeg- including lactic acid bacteria (LAB), yeast, and fungi to radation pathway. However, the toxins might be easily remove mycotoxins from food (Abrunhosa et  al. 2002; released back and this depends on the stability of the Assaf et  al. 2018a, b, c; Assaf et  al. 2019a; El-Nezami complex formed between the bacterial surface and the et  al. 2004a, b, El-Nezami et  al. 1998). In addition, the toxins (Solis-Cruz et al. 2019). use of microorganisms’ enzymes and their metabolites also showed efficiency in the mycotoxin degradation Bacteria processes (Karlovsky 1999; Li et al. 2020). The biological Many studies have reported that bacteria are useful bio- methods used in the removal and degradation of myco- logical agents for mycotoxin detoxification. Bacteria toxins are attractive and environmentally friendly and can remove mycotoxin by biosorption or biodegrada- therefore may offer better substitutes to the chemical tion mechanisms. A summary of the literature reporting and physical methods (Assaf et al. 2018a, b, c; Assaf et al. bacterial strains for mycotoxins detoxification in various 2019a). media is presented in Table  1. The removal percentage This review aims to discuss the biological decontami - of many mycotoxins involving various bacterial strains nation of mycotoxins and to review the mechanisms of reached a high efficiency of up to 94%. detoxification by yeasts and bacteria, in addition to bac - It was demonstrated that the use of Generally Recog- terial biofilms and their enzymes. Moreover, this review nized as Safe (GRAS) probiotic bacteria such as LAB is presents the contribution of biological detoxification very promising in mycotoxins detoxification (Abdelmo - methods to food safety and consumers’ health. tilib et al. 2018; El-Nezami et al. 1998; Fuchs et al. 2008; Assaf et  al. 2019a; Assaf et  al. 2018a, b, c; Ben Taheur Biological detoxification of mycotoxins using et  al. 2019; Wang et  al. 2018a, b). Haskard et  al. (2001) microorganisms revealed that several LAB has been established to detox- The biological detoxification of mycotoxins is defined ify AFB which is the most potent human carcinogen. as the usage of microorganisms, as well as their micro- Haskard and his team have assessed the ability of five bial enzymes and metabolites for mycotoxins binding Lactobacillus strains: L. rhamnosus GG, L. rhamnosus Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 3 of 14 Table 1 Mycotoxins removal percentage of different bacterial strains Strain Mycotoxins Sample Removal (%) References Lactobacillus acidophilus VM20 OTA Liquid medium 97 (Fuchs et al. 2008) Lactobacillus bulgaricus OTA PBS 94 ( Varga et al. 2005) Lactobacillus plantarum PAT Apple juice 91.2 (Zoghi et al. 2017) Lactobacillus rhamnosus LC705 AFB PBS 87.8 (Haskard et al. 2001) Lactobacillus rhamnosus GG AFB PBS 84.1 (Haskard et al. 2001) Lactobacillus kefiri KFLM3 OTA Milk 81 ( Taheur et al. 2017) Lactobacillus rhamnosus 6224 PAT Apple juice 80.4 (Hatab et al. 2012) Bifidobacterium animalis VM 13 PAT Liquid medium 80 (Fuchs et al. 2008) Lactobacillus rhamnosus 1088 AFB PBS 79 (Chlebicz and Śliżewska 2020) Lactobacillus rhamnosus GG ZEN PBS 70 (El-Nezami et al. 2002) Enterococcus faecium 21,605 PAT Apple juice 64.5 (Hatab et al. 2012) Lactobacillus rhamnosus GG AFM PBS 63.1 (Assaf et al. 2017) Lactobacillus rhamnosus GG biofilm AFM Milk 60.7 (Assaf et al. 2019a) Actinobacteria AT8 OTA PBS 52.6 (El Khoury et al. 2017) Lactobacillus plantarum 13 M5 PAT Apple juice 43.8 ( Wei et al. 2020) Lactobacillus plantarum VM 37 OTA Liquid medium 43 (Fuchs et al. 2008) Lactobacillus plantarum VM 37 PAT Liquid medium 39 (Fuchs et al. 2008) LC705, L. acidophilus, L. gasseri, and L. casei to remove Mycotoxins binding in several studies was reported AFB from liquid media and have demonstrated that the to be rapid, and the binding percentages were generally probiotic strains L. rhamnosus GG and L. rhamnosus affected by many factors such as incubation time, type of LC705 were highly effective in detoxifying of up to 80% bacteria, bacterial concentration, pH, type of medium, AFB (Haskard et al. 2001). Additionally, El-Nezami et al. and temperature (El-Nezami et  al. 2004a). The use of (2002) have shown that L. rhamnosus GG was able to bacterial adsorbents in beverages presents several advan- remove up to 70% of ZEN from liquid media. Fuchs et al. tages over chemical and physical detoxification methods. (2008) showed that Bifidobacterium animalis strain VM The bacterial detoxification assay is considered more 12 was able to remove approximately 80% of PAT and L. effective and highly specific, especially since the binding acidophilus strain (VM 20) reduced the OTA levels by affinity of mycotoxins varies not only among different more than 90% among all tested strains. species but also among different strains within the same Other strains of bacteria have been investigated for species. Furthermore, the use of several probiotic bacte- their binding capability to mycotoxins. El Khoury et  al. ria has made the bacterial detoxification process safer. (2017) have investigated the ability of actinobacteria, which are found in soil habitat and comprise the larg- Yeasts est bacterial genera “Streptomyces”, to bind and detoxify Studies showed that probiotic yeasts or products con- OTA. El Khoury et al. (2017) have established that seven taining yeast cell walls can remove mycotoxins from different strains of actinobacteria were able to bind OTA beverages (Pizzolitto et  al. 2012). A summary of the lit- to different extents. Among the tested strains, AT8 strain erature in which yeast strains were used for mycotox- was remarkably able to detoxify OTA to up to 52.61%. ins detoxification is presented in Table  2. Generally, it Also, Verheecke et al. (2014) have found that the mutual is well established that S. cerevisiae is extensively used interaction between Streptomyces spp. (27 strains) and in biotechnology processes such as baking and distill- Aspergillus flavus (NRRL 62477) can reduce the level of ing industries. Some studies shown that S. cerevisiae AFB and AFB in vitro to up to 73%. In 2018, Wang et al. can remove OTA from microbiological media and other 1 2 (2018a, b) have shown that Lysinibacillus sp. strain, iso- beverages (Piotrowska and Masek 2015). Other studies lated from chicken large intestine digesta, demonstrated have demonstrated that S. cerevisiae is most effective in high ability in removing ZEN. Additionally, Taheur et al. AFB binding (Corassin et al. 2013). Corassin et al. (2013) (2017) have proved that Lactobacillus kefiri, Kazach- have demonstrated that heat-killed S. cerevisiae cells have stania servazzii, and Acetobacter syzygii were able to the potential to reduce AFM levels in milk. Other yeast remove up to 100% of AFB . strains such as Kluyveromyces Lactis and Kazachstania 1 Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 4 of 14 Table 2 Mycotoxins removal percentage of different yeast strains Strain Mycotoxins Sample Removal (%) References S. cerevisiae AFM UHT skim milk 90.3 (Corassin et al. 2013) S. cerevisiae RC008 OTA YPD broth 82.3 (Armando et al. 2012) S. cerevisiae AFM PBS 78.7 (Abdelmotilib et al. 2018) S. cerevisiae YS3 PAT Apple juice 72.6 (Yue et al. 2011) Kluyveromyces Lactis AFM PBS 69.1 (Abdelmotilib et al. 2018) Kazachstania servazzii KFGY7 OTA Milk 62 ( Taheur et al. 2017) S. cerevisiae 0068 AFB PBS 46.7 (Chlebicz and Śliżewska 2020) servazzii KFGY7 also showed removal ability of mycotox- microorganisms is a rapid process, which forms a revers- ins from milk reaching to up to 69.14%. ible complex between the toxin and the bacterial surface without altering the mycotoxins’ structure (Bueno et  al. Chitin and shrimp shells 2007). Shetty and Jespersen’s investigations revealed that Both polysaccharides and peptidoglycans are found in the detoxification process is related to a physical union the cell wall of different microorganisms and have been between the mycotoxins and the bacterial cell compo- shown to be involved in mycotoxin binding (Kim et  al. nents, instead of covalent binding or biodegradation by 2017). The amino sugar N-acetyl-D-glucosamine (Glc - bacterial metabolism (Shetty and Jespersen 2006). Yian- NAc) is the key component of the cell wall of microor- nikouris et  al. (2006) reported that hydrogen bonds and ganisms including fungi, bacteria, and yeast (Chen et  al. Van der Waals interactions may be implicated in this 2010), and this has been mainly responsible for the binding mechanism. On the other hand, according to detoxification of mycotoxins (Assaf et  al. 2018a , b, c). Hernandez-Mendoza et  al. (2009), the differences in This sugar is also found in the exoskeleton of crustaceans the mycotoxins’ binding ability of various Lactobacillus in the form of a polymer known as “chitin”, specifically in strains could be explained by the differences in the cell shrimp shells (Xu et al. 2008; Iqbal et al. 2017) that con- wall components specifically teichoic acid and pepti - tain primarily 30–40% of chitin (Venugopal 2016). In that doglycan contents. Different structures in the cell wall of sense, attention has been given to chitinous polymers microorganisms are responsible for the mycotoxin bind- and shrimp shells and their ability to remove mycotox- ing capacity. Cell walls comprise carbohydrates (pep- ins. Assaf et al. (2018a, b, c) have evaluated the ability of tidoglycan, mannose, and glucan), proteins, and lipids, chitin (as a natural biopolymer) and ground shrimp shells which may offer different binding sites (Wang et  al. (which contain 30–40% of chitin) to detoxify A FM . They 2019a, b). However, there are arguments among different showed that chitin and shrimp shells were able to bind researches on the specific cell wall components impli - AFM in milk at varied binding percentages in the range cated in the binding processes, such as glucogalactans of 14.29 and 94.74%. Yearly, up to 8 million tons of crab, and β-glucans (Taheur et  al. 2017), mannoproteins shrimp, and lobster shells are wasted worldwide, (Yan (Caridi et  al. 2012), β- glucans and mannans (Pereyra and Chen 2015) thus, valorisation of these wastes, to be et al. 2015). Therefore, in the interaction of bacterial cells used as potential biosorbents in mycotoxin detoxification and mycotoxins, it appears that various binding mecha- would contribute to decreasing food waste and eliminat- nisms may be implicated involving non-covalent bond- ing toxic effects on humans. They would also be of great ing, hydrophobic interactions, ionic interactions, or interest as an added benefit to the food industry. hydrogen bonds, (Huwig et al. 2001; Ringot et al. 2007). The cell wall portion of S. cerevisiae is mostly com - Mechanisms of action involved through microbial binding posed of polysaccharides with an inner layer of β-D- To date, there are two theories by which LAB elimi- glucans chains, which constitute 50 to 60% of the wall’s nates toxins: one through physical adsorption and the dry weight (Jouany et  al. 2005). Jouany et  al. (2005) other through biodegradation of mycotoxins. Research- have shown that β-D-glucans are the components ers have conducted several detoxification experiments mainly responsible for the complexation of ZEN. Also, to test which theory is more adequate. Experiments they showed that the chemical interaction is more of an with thermally inactivated bacteria provoked higher adsorption type than binding, where both weak hydro- detoxification of mycotoxins as compared to activated gen bonds and Van der Waals interactions are involved cells. Studies showed that the binding of mycotoxins by in this adsorption. Moreover, it has been demonstrated Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 5 of 14 Detoxification approaches of mycotoxins by biofilms that the binding process of OTA to the surface of living Bacteria exist in nature under two forms: either as freely or dead yeast cells, is achieved, in general, by adsorp- swimming planktonic bacteria, or as sessile in attached tion mechanisms (Bejaoul et  al. 2004). These research - colonies of microorganisms forming a biofilm. Thus, ers have concluded that the yeast cell wall and its the biofilm may be considered as “a three-dimensional charge are involved in the adsorption process (Bejaoul structure of sessile microorganisms that are irreversibly et  al. 2004). These observations were similar to those attached to biotic or abiotic surfaces, embedded in self- of Piotrowska (2014) who found that bacteria, with formed extracellular polymeric substances (EPS) (Lewan- partially removed cell walls, had less ability to bind dowski and Boltz, 2010). OTA, as compared to the bacteria with intact cell walls In the last decades, biofilm formation has been impli - (Piotrowska 2014), highlighting, therefore, the impor- cated in many industrial and domestic domains (Roger tance of the cell wall in the adsorption mechanisms et al. 2008). Salas-Jara et al. (2016) have studied the abil- (Piotrowska 2014). ity of some strains of LAB to form a biofilm and Lebeer The properties of the bacterial cell surface play a et  al. (2007) have shown the ability of L. rhamnosus GG vital role in the binding mechanism. In another study, to form biofilm on polystyrene support. Recently, a new involving Escherichia coli, a Gram-negative bacterium, method was developed for the detoxification of milk it was established that it was incapable of removing from AFM by using L. rhamnosus GG biofilm (Assaf mycotoxins due to its moderately hydrophilic nature et  al. 2019a). The biofilm was formed on polystyrene and its present surface components (lipopolysaccha- petri plates and in polyethylene tubes. The detoxification rides) (Pierides et  al. 2000). On the other hand, LAB process was carried out using the biofilm formed on day bacteria having hydrophobic sites on their cell surface 3, which is considered a highly attached biofilm and an were confirmed to have the ability to bind OTA (El- efficient binding agent. The percentages of bound AFM Nezami et  al. 1998). Assaf et  al. (2019a) hypothesized by L. rhamnosus GG biofilm reached to up to 60.7%. that the biofilm matrix may be involved in AFM bind- Moreover, the quality of milk after A FM detoxification ing rather than the bacterial cells themselves. Addi- had no significant changes in the protein content, but tionally, this study observed that washing the biofilm some changes in fat and total dry matter contents ratio. had released some fraction of the weakly bound AFM . Additionally, Assaf et  al. (2019a) have studied the stabil- This confirms that binding is reversible due to the dis- ity of the AFM -biofilm complex using different AFM ruption of some electrostatic bonds as hydrogen bonds 1 1 concentrations. The study has shown that the binding and Van der Waals interactions (Hernandez-Mendoza was reversible and a portion of the bound A FM was et al. 2009). released after successive washings. To date, this tech- Moreover, higher mycotoxins’ elimination was shown nique is a modern technique that relies on the removal of by inactivated bacterial cells. For example, Haskard mycotoxins by a biofilm, making it of great challenge and et  al. (2001) found that high temperature leads to pro- appeal, especially to those that are interested in remov- tein denaturation in the bacterial cell wall, and this ing mycotoxins from foods. However, the use of biofilms results in the generation of pores, that facilitate further as a technique of detoxification of mycotoxins is still in aflatoxins’ adsorption and mycotoxins elimination. its early stages and additional studies that might be of a Additionally, the same authors suggested that protein potential usefulness to food industries should be con- denaturation might increase the hydrophobic nature ducted. Hence, on a general note, using biofilms as bio - of the surface or form Maillard reaction products and logical adsorbents for mycotoxins may be considered as such alterations allow aflatoxins to bind to the bacterial a solid base for the progress of biological detoxification cell wall and plasmatic membrane components, which methods. were masked when the cell wall was intact (Haskard et  al. 2001). Chlebicz and Śliżewska (2020) recently Detoxification approaches of mycotoxins by microbial have shown that treatment of yeasts by heat and acid- enzymes ity improved significantly OTA detoxification by up to Enzymatic detoxification is one of the most promis - 75% from liquid medium compared to untreated cells. ing methods of mycotoxins control, especially that it is Expecting that both polysaccharides and peptidogly- devoid of some significant disadvantages that chemical cans are affected by heat and acid treatments, these methods employ such as chemical contamination of raw researchers postulated that acidic treatments could materials, nutrient loss, time-consuming and expensive disturb polysaccharides, by releasing monomers that (Wang et al. 2019a, b). A wide range of microorganisms are broken down into aldehydes, which could lead to including bacteria, molds, and yeasts are involved in more adsorption sites than viable cells (Chlebicz and the enzymatic detoxification of mycotoxins (Hathout Śliżewska 2020). Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 6 of 14 and Aly 2014). Generally, microbial enzymes are able to The mycotoxins detoxification efficacy of different metabolize, destroy or inactivate mycotoxins into less enzymes produced as part of the yeasts/fungi metabolic or nontoxic metabolites (Lyagin and Efremenko 2019). activity are summarized in Table 3. Degradation is a process by which most of the micro- In one of the first studies to be conducted on microbial organisms use during their life activities to degrade enzymes, manganese peroxidase can serve as a good can- certain substances converting them into less or even didate for detoxifying various types of mycotoxins (Wang non-toxic products. During the degradation process, et  al. 2011). This peroxidase, purified from different lig - the vital active molecules secreted by microorganisms nocellulose-degrading fungi such as Irpex lacteus, Phan- are enzymes (Guan et al. 2021). erochaete chrysosporium, Ceriporiopsis subvermispora, Most of the scientific studies to date are dedicated to and Nematoloma frowardii, can degrade AFB , ZEN, and enzymatic degradation for detoxifying the most notable other mycotoxins (Tang et al. 2013). Loi et al. (2018) have mycotoxins, including AF, OTA, ZEN, TCT, and PAT described the ability of laccase purified from Pleurotus (Tang et  al. 2013; Loi et  al. 2018; Zhang et  al. 2020). eryngii to simultaneously degrade A FB and ZEN by 86% Several microbial enzymes from bacteria, yeast, and and 100% respectively. fungi that are capable of performing various modifica - Interestingly, Bacillus pumilus ES-21 was able to tions or transformations of mycotoxins have been iso- degrade 95.7% of ZEN into 1-(3,5-dihydroxyphenyl)- lated and investigated (Ben Taheur et al. 2019). 6-hydroxy-l-undecen-l0-one (Wang et  al. 2017). Overall, Examples of microbial enzymes, reported in the lit- three kinds of enzymes have been identified to degrade erature, involved in mycotoxins degradation are pre- ZEN: Lactonase (Bi et al. 2018; Wang et al. 2018a, b), per- sented in Table  3. Studies have shown that some oxidase (Tang et  al. 2013), and laccase (Loi et  al. 2018). enzymes from yeasts have important characteristics Lactonase ZHD101 was mostly proposed for its high that enable them to transform toxins into less toxic efficiency in ZEN degrading ability, found in S. cerevisiae ones (Schatzmayr et  al. 2006; Halász et  al. 2009). A (Takahashi-Ando et  al. 2002) and L. reuteri (Yang et  al. number of enzymes belonging to Aspergillus species are 2017). Even though lactonase has high degrading abil- found to be involved in aflatoxin degradation. Further - ity, however, it is not highly thermostable which restricts more, Aspergillus niger, an isolate from feed samples, its applications (Zhang et al. 2020). Recently, Wang et al. was shown to biodegrade AFB (Zhang et  al. 2014). (2018a, b) identified a lactonohydrolase enzyme, Zhd518, Other fungal strains that may contribute to the detoxi- which exhibited high degrading activity against ZEN. The fication of aflatoxins, by secreting oxidative enzymes same authors reported that Zhd518 could be an excel- such as laccase and manganese peroxidase have been lent candidate for ZEN detoxifying due to its high spe- reported (Alberts et  al. 2009). Interestingly, manga- cific activity against ZEN and its derivatives (Wang et al. nese peroxidase extracted from Phanerochaete sordida 2018a, b). Recently, Zhang et  al. (2020) have identified was responsible for eliminating 86% of A FB in  vitro, an effective ZEN-degrading lactonase from Gliocladium increasing to 100% with successive additions of the roseum, named ZENG for the first time (Zhang et  al. enzyme (Wang et  al. 2011). Moreover, laccase enzyme 2020). This recombinant enzyme has great activity and purified from Trametes versicolor was able to remove stability at a pH of 7.0., characterized by its great detoxi- 67% of AFB (Zeinvand-Lorestania et al. 2015). fication ability of ZEN and its derivatives, α-zearalenol Recently, Zhang et al. (2018) showed that the intracel- (α-ZOL), and α-zearalanol (α-ZAL) (Zhang et al. 2020). lular enzymes of Y. lipolytica Y-2 were able to degrade OTA more rapidly than its viable cells (Zhang et  al. Mechanisms of action involved in the enzymatic 2018). Also, Chang et al. (2015) have reported that car- transformation of mycotoxins boxypeptidase, an enzyme purified from B. amylolique - Many biochemical transformation reactions of myco- faciens ASAG1 was capable of reducing OTA by 72%. toxins by microorganisms and their enzymes have been Additionally, the enzymatic extracts from Rhodoc- described such as acetylation, glucosylation, ring cleav- occus erythropolis, N. corynebacterioides DSM 20151, age, hydrolysis, sulfation, deamination, and decarboxy- and M. fluoranthenivorans sp. nov. DSM 44556 T have lation (Li et  al. 2020). Some of the biotransformation revealed more than 90% degradation capability of reactions of mycotoxins by some microbial enzymes are AFB (Hackbart et al. 2014). Recently, Shu et al. (2018) shown in Table 4. established that heat-treated supernatant from Bacil- lus velezensis DY3108 was able to degrade 94.7% of Application of biological detoxification processes AFB into less toxic metabolites. Recently, it was found in the food industry that Bacillus pumilus was able to degrade 88% of A FB Many microorganisms have been proposed for use as (Sangi et al. 2018). detoxifying agents in food and feed, but only few have Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 7 of 14 Table 3 Examples of some types of biotransformation reactions and the involved microorganisms or enzymes Type of Bio- Hydrogenation Hydroxylation Sulfation Reduction of the ketonic carbonyl Transformation group Reaction Substrate Product Microorganism or Penicillium raistrickii Phenylobacterium Sphaerodes mycoparasitica Rhizopus sp., Aspergillus sp Enzyme References (Wu et al. 2009) (Wegst and Lingens 1983) (Kim and Vujanovic 2017) (Brodehl et al. 2014) Type of Bio- Hydrolysis Oxido-Reduction Reduction of Carbonyl group Transformation Reaction Substrate Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 8 of 14 Table 3 (continued) Type of Bio- Hydrogenation Hydroxylation Sulfation Reduction of the ketonic carbonyl Transformation group Reaction Product Microorganism or Aspergillus niger/ Lipase Bacillus pumilus ES-21 /purified lactonase Lactobacillus plantarum Aspergillus niger, Eurotium herbariorum, Enzyme Rhizopus sp. References (Stander et al. 2000) (Xu et al. 2016; Wang et al. 2017) (Soukup et al. 2016) (Nakazato et al. 1991) Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 9 of 14 Table 4 Examples of enzymes and their microorganism origin that are involved in the degradation of mycotoxins Microbial Origin Name of enzyme Mycotoxins Degradation (%) References Or Type of enzyme Aspergillus niger MUM 03.58 Carboxypeptidase OTA 99 (Abrunhosa et al. 2006) Bacillus amyloliquefaciens ASAG1 Carboxypeptidase OTA 72 (Chang et al. 2015) Aspergillus tubingensis M036 – OTA 97.5 (Cho et al. 2016) Aspergillus tubingensis M074 – OTA 91.3 (Cho et al. 2016) Aspergillus niger Ochratoxinase OTA ND (Dobritzsch et al. 2014) Yarrowia lipolytica Y-2 Carboxypeptidases OTA ND (Zhang et al. 2018) Phanerochaete sordida Manganese peroxidase AFB 86 ( Wang et al. 2011) Trametes versicolor Laccase AFB 67 (Zeinvand-Lorestania et al. 2015) Pleurotus eryngii Laccase AFB 86 (Loi et al. 2018) Pleurotus eryngii Laccase ZEN 100 (Loi et al. 2018) Escherichia coli Lactonohydrolase Zhd518 ZEN ND ( Wang et al. 2018b) lignocellulose-degrading fungi Manganese Peroxidase ZEN 34.0 ( Tang et al. 2013) lignocellulose-degrading fungi Manganese Peroxidase AFB 84.9 ( Tang et al. 2013) Rhodococcus erythropolis – AFB 90 (Hackbart et al. 2014) Bacillus velezensis DY3108 – AFB 94.7 (Alberts et al. 2009) Bacillus pumilus – AFB 88 (Alberts et al. 2009) Bacillus pumilus ES-21 – ZEN 95.7 ( Wang et al. 2017) Gliocladium roseum ZENG ZEN 60 (Zhang et al. 2020) Aspergillus niger – AFB 23.6 (Zhang et al. 2014) Peniophora sp. SCC0152 – AFB 40.45 (Alberts et al. 2009) been further investigated for uses in the food indus- samples where the highest detoxification percentage try. Many factors should be considered while selecting reached was 81.3% without altering the physicochemical a binder for mycotoxins, particularly in the food sector, properties of milk. Further optimization of the bio-filters including non-pathogenicity, specificity, effective seques - may subsequently lead to different practical detoxifica - tering and the absence of adverse effects. tion applications of various mycotoxins from dairy prod- Assaf et  al. (2018a, b, c) have proposed a novel ucts and beverages. machine that may be employed in the detoxification In a previous study, Hatab et al. (2012) showed that L. of mycotoxin from liquid beverages. This machine rhamnosus 6224 and Enterococcus faecium 21,605 were has probiotic LAB biofilms fixed to a customized car - able to remove 80.4 and 64.5% of patulin (PAT) from tridge; accordingly, it allows liquid food to pass through apple juice, respectively. These researchers have proved these adsorbents which results in detoxified liquid. The that LAB could be used as a novel and promising adsor- prototype of the invested detoxifying machine is pre- bent to bind PAT without altering the quality of the juice. sented in Fig.  1. Many aspects, such as the flow rate of Yue et al. (2011) have shown that inactivated S. cerevi- the pump, the number of cartridges utilized, the kind siae YS3 powder was able to remove up to 72.61% of PAT of biological adsorbents are proposed to be explored from apple juice, and additionally, there was no negative throughout the development of this machine prototype. impact on the quality of apple juice, based on the quality This machine has the potential to be a promising appli - parameters measured, such as degrees Brix, total sugar, cation in liquid food purification, particularly because titratable acidity, color value, and clarity. This study sug - the creation of biofilms is cost-effective, however, it is gests that the inactivated S. cerevisiae YS3 powder could also very important to assess the effect of this treat - be a hopeful binder of PAT in apple juice, especially since ment on the organoleptic characteristics of the bever- yeast has low cost, high biomass properties, and can be ages after detoxification process. simply separated from apple juice (Yue et al. 2011). Lately, Foroughi et al. (2018) have suggested a method Although many articles on mycotoxin elimination to detoxify AFM -contaminated milk by immobilizing by adsorption and transformation have been pub- yeast such as S. cerevisiae on perlite support. The results lished, their applicability in the food industry has been revealed a high significant removal of AFM from milk restricted. This might be attributed to a lack of knowledge 1 Nahle et al. International Journal of Food Contamination (2022) 9:3 Page 10 of 14 Fig. 1 Prototype machine for detoxification of mycotoxins from beverages using biological adsorbents regarding transformation processes, the toxicity of trans- identifying the transformed products, and (ii) performing formation products, and the influence of transformation toxicity assays on the resultant intermediate metabolites reactions on the nutritional content of food and feed. and products. Meanwhile, because the enzyme’s genetic Degraded products have not been recognized in certain sequence is known, molecular engineers might improve circumstances and so cannot be employed in industrial the enzyme’s selectivity and catalytic performance by operations. making changes to the active region. All of these per- Recently, Zhang et  al. (2020) have identified a potent ceptions should be taken into account in order to aid in enzyme, ZENG, that is efficient in detoxifying up to 60% the mitigation of mycotoxins. Biological degradation of of ZEN and its toxic derivatives. However, most enzymes mycotoxins is a promising method that can be further do not meet the requirements of industrial applications developed by focusing on the isolation of specific micro - due to their low ability to withstand high temperatures organisms, optimizing their growth, and creating condi- (Atalah et  al. 2019). So thermostability is an important tions that favor massive production of enzymes. characteristic of industrial enzymes and to meet the industrial demands, efforts should also seek to provide Conclusion highly thermostable enzymes, which can reduce the cost Mycotoxins have received much attention due to their of production, develop its efficiency, and help in lowering severe impact on human and animal health. Their microbial contamination in industrial approaches. detoxification has been always the goal of research. Although, an enzymatic catalysis is a promising While biological detoxification of mycotoxins has been approach that can be used to detoxify mycotoxins (Ben widely studied, little is still known about the potential Taheur et  al. 2019). However, not all mycotoxins’ modi- applications in the food, feed, and beverages industries. fications and transformations can lead to detoxification So practically, scientists should focus on the potential products. For example, Hahn et  al. (2015) showed that use of microorganisms in the detoxification of myco - the α- and/or β-ZOL, the reduced products of ZEN, have toxin mixtures from food and beverages. In addition, it similar estrogenic activity compared to ZEN. Karabulut is of utmost importance to analyze the physicochemi- et  al. (2014) deduced that aflatoxicol, the reduced prod - cal profile, sensory properties, and organoleptic char - uct of AFB , has a similar ability to form an exo-epoxide acteristics of the juices and food after detoxification of analog that binds to DNA. mycotoxins. Further, it is necessary to isolate and select Enzymatic detoxification, in our opinion, might be a suitable enzymes and microorganisms for efficient viable technique for the majority of mycotoxins if applied detoxification and to analyze the enzymatic properties properly. The efficacy of the biodegradation process can and their catalytic processes in food and beverages. be validated by using two criteria: (i) discovering and In brief, what makes a good binder is its adsorption Nahle  et al. International Journal of Food Contamination (2022) 9:3 Page 11 of 14 Received: 12 December 2021 Accepted: 23 March 2022 capacity, specificity, safety, and stability. Therefore, after the future development of these promising approaches, enzymes and microorganisms can be used as food and feed additives or as detoxifying agents during food pro- References cessing, while preserving the nutritional and organo- Abrunhosa L, Serra R, Venâncio A (2002) Biodegradation of ochratoxin A by leptic quality of food commodities and beverages. fungi isolated from grapes. J Agric Food Chem 50:7493–7496. https:// doi. org/ 10. 1021/ jf025 747i Abdelmotilib NM, Of C, Applications T, Hamad G, Salem EG (2018) Aflatoxin M1 reduction in Milk by a novel combination of probiotic bacterial Abbreviations aflatoxin M1 reduction in Milk by a novel combination of probiotic AFs: Aflatoxins; OTA: Ochratoxin A; PAT: Patulin; ZEN: Zearalenone; TCT : Tri- bacterial and yeast strains. Nutr food Saf 8:83–99. https:// doi. org/ 10. chothecenes; LAB: Lactic Acid Bacteria; AFB : Aflatoxin B ; AFM : Aflatoxin M ; 1 1 1 1 9734/ ejnfs/ 2018/ 39486 PBS: Phosphate Buffer saline; AFB : Aflatoxin B ; GRAS: Generally Recognized 2 2 Abrunhosa L, Santos L, Venâncio A (2006) Degradation of Ochratoxin A by as Safe; EPS: Extracellular Polymeric Substances; α-ZOL: α-zearalenol; α-ZAL: proteases and by a crude enzyme of aspergillus Niger. Food Biotechnol α-zearalanol. 20:231–242 Alberts JF, Gelderblom WCA, Botha A, van Zyl WH (2009) Degradation of Acknowledgments aflatoxin B1 by fungal laccase enzymes. Int J Food Microbiol 135:47–52. This work was supported by the Conflicts of Interest research council and the https:// doi. org/ 10. 1016/j. ijfoo dmicro. 2009. 07. 022 research and analysis center (CAR) at the Faculty of Sciences in Saint-Joseph Armando MR, Pizzolitto RP, Dogi CA, Cristofolini A, Merkis C, Poloni V, Dalcero University (USJ ) and the Lebanese University through a grant 6341/4. AM, Cavaglieri LR (2012) Adsorption of ochratoxin A and zearalenone by potential probiotic Saccharomyces cerevisiae strains and its relation Authors’ contributions with cell wall thickness. J Appl Microbiol 113:256–264. https:// doi. org/ Sahar Nahle: Original draft preparation-Writing-Reviewing and Editing. Andre 10. 1111/j. 1365- 2672. 2012. 05331.x El Khoury: Reviewing-Editing. Ali Chokr: Reviewing-Editing. Nicolas Louka: Assaf JC, Atoui A, El Khoury A, Chokr A, Louka N (2017) A comparative study of Reviewing-Editing. Ioannis Savvaidis: Reviewing-Editing and Ali Atoui: Struc- procedures for binding of aflatoxin M1 to Lactobacillus rhamnosus GG. turing/Formulation, Reviewing-Editing. The author(s) read and approved the Brazilian J Microbiol 49:120–127. https:// doi. org/ 10. 1016/j. bjm. 2017. final manuscript. 05. 003 Assaf JC, El Khoury A, Atoui A, Chokr A (2018b) A novel process for detoxifica- Authors’ information tion of liquid foods from mycotoxins SN is a Ph.D. student between the Lebanese University and the Université Assaf JC, El Khoury A, Atoui A, Louka N, Chokr A (2018c) A novel technique for Saint-Joseph de Beyrouth. aflatoxin M1 detoxification using chitin or treated shrimp shells&nbsp;: AK is a Professor at the Faculté des Sciences, Université Saint-Joseph de in vitro effect of physical and kinetic parameters on the binding stabil- Beyrouth. ity. Appl Microbiol Biotechnol 102:6687–6697 IS is a Professor at the Department of Environmental Health Sciences, Univer- Assaf JC, Louka N, El Khoury A, Chokr AAA (2018a) A novel process for detoxifi- sity of Sharjah. cation of liquid foods from mycotoxins AC is a Professor at the Department of Life and Earth Sciences, Faculty of Sci- Assaf JC, El Khoury A, Chokr A, Louka N, Atoui A (2019a) A novel method for ences, Lebanese University. elimination of aflatoxin M1 in milk using Lactobacillus rhamnosus GG NL is a Professor at the Faculté des Sciences, Université Saint-Joseph de biofilm. Int J Dairy Technol 72:248–256. https:// doi. org/ 10. 1111/ 1471- Beyrouth. 0307. 12578 AA is a Professor at the Department of Life and Earth Sciences, Faculty of Sci- Assaf JC, Nahle S, Chokr A, Louka N, Atoui A, El Khoury A (2019b) Assorted ences, Lebanese University. methods for decontamination of aflatoxin M1 in Milk using microbial adsorbents. Toxins (Basel) 11:304 Funding Atalah J, Cáceres-Moreno P, Espina G, Blamey JM (2019) Thermophiles and the This review paper is based upon work supported by the Lebanese University applications of their enzymes as new biocatalysts. Bioresour Technol through a grant 6341/4. 280:478–488. https:// doi. org/ 10. 1016/j. biort ech. 2019. 02. 008 Battilani P, Toscano P, Van Der Fels-Klerx HJ, Moretti A, Camardo Leggieri M, Availability of data and materials Brera C, Rortais A, Goumperis T, Robinson T (2016) Aflatoxin B 1 con- Not applicable. tamination in maize in Europe increases due to climate change. Sci Rep 6:1–7. https:// doi. org/ 10. 1038/ srep2 4328 Declarations Bejaoul H, Mathieu F, Taillandier P, Lebrihi A (2004) Ochratoxin A removal in synthetic and natural grape juices by selected oenological Saccharo- Competing interests myces strains. J Appl Microbiol 97:1038–1044. https:// doi. org/ 10. 1111/j. 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Journal

International Journal of Food ContaminationSpringer Journals

Published: Apr 25, 2022

Keywords: Detoxification; Mycotoxins; Microorganisms; Biofilm; Enzymatic degradation

References