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Potentials of termite mound soil bacteria in ecosystem engineering for sustainable agriculture

Potentials of termite mound soil bacteria in ecosystem engineering for sustainable agriculture The environmental deteriorating effects arising from the misuse of pesticides and chemical fertilizers in agriculture has resulted in the pursuit of eco-friendly means of producing agricultural produce without compromising the safety of the environment. Thus, the purpose of this review is to assess the potential of bacteria in termite mound soil to serve as biofertilizer and biocontrol as a promising tool for sustainable agriculture. This review has been divided into four main sections: termite and termite mound soils, bacterial composition in termite mound soil, the role of bacteria in termite mound soil as biofertilizers, and the role of bacteria in termite mound soil as biocontrol. Some bacteria in termite mound soils have been isolated and characterized by various means, and these bacteria could improve the fertility of the soil and suppress soil borne plant pathogens through the production of antibiotics, nutrient fixation, and other means. These bacteria in termite mound soils could serve as a remarkable means of reducing the reliance on the usage of chemical fertilizers and pesticides in farming, thereby increasing crop yield. . . . . Keywords Biofertilizers Chemical fertilizers Environmental safety Food security Organic farming Introduction which will certainly increase as human population increases, it is therefore paramount to produce agricultural produce in a sus- tainable manner without causing any harm to the environment Traditional agriculture contributes a key part in meeting the demand for food of a rising human populations (Santos et al. (Pathak et al. 2018). To achieve this, eco-friendly methods like 2012) that is currently more than seven billion people globally, the use of biofertilizers and biocontrols need to be employed to and this figure is expected to rise to eight billion by 2020 boost soil fertility and suppress soil plant pathogens (Igiehon (Conway 2012). The use of pesticides and inorganic fertilizers and Babalola 2017). Biofertilizers are substances that are made to boost the fertility of soil and control plant pests has increased up of live microorganisms (which could be plant growth- food production; however, their misuse has resulted in eutrophi- promoting rhizobacteria (PGPR)) which when applied to soil, cation of water bodies, air, and groundwater pollution, thus plant, or seeds, inhabit the rhizosphere of plants and stimulate affecting human and environmental health (Savci 2012;Alori plant growth (Malusá and Vassilev 2014). PGPR enrich the soil et al. 2017). The prolonged use of these chemicals affects soil by through potassium solubilization, phosphate mineralization, and reducing its water-holding capacity, increasing soil salt content, nitrogen fixation, breaking down organic substances to a form leading to inequality of soil nutrient distribution, and ultimately that plants can utilize. Further, they help in the regulation of affecting the structure and fertility of soil (Savci 2012). Looking plant growth substances and the production of antibiotics that at these negative effects of chemical fertilizers and pesticides, suppress soil borne plant pathogens (they are microscopic or- ganisms that prefer to live within the soil causing harm to plants and even soil itself) such as virus, bacterium, fungus, or nema- * Olubukola Oluranti Babalola tode (Liu et al. 2018; Parewa et al. 2018) that cause damaging olubukola.babalola@nwu.ac.za effects on fruits and growing and stored crops of economic Ben Jesuorsemwen Enagbonma importance, therefore leading to plant diseases which contribute enagbonma30@yahoo.com directly to losses in agriculture (Widmer 2014). Investigations associated with soil uniqueness in controlling Food Security and Safety Niche, Faculty of Natural and Agricultural soil microbial community composition could enlighten our un- Sciences, North-West University, Private Mail Bag X2046, derstanding of soil quality and biogeochemical processes (Li Mmabatho 2735, South Africa 212 Ann Microbiol (2019) 69:211–219 et al. 2015). The structures and functions of soil microorgan- (Jouquet et al. 2015; Vidyashree et al. 2018). Termites feed isms are widely used as a pointer to assess the degree of soil on plant materials, fungi, and humus, and because of their health (Zhu et al. 2017). This is because soil microorganisms feeding habit, they are considered as a big menace to agricul- function as a means of transforming carbon-based materials, tural produce in sub-tropical and tropical areas (Rosengaus cycling minerals, and energy and also perform further roles that et al. 2011; Negassa and Sileshi 2018). This is because they could advance soil health and agricultural sustainability have the tendency of destroying growing or stored crops and (Choudhary et al. 2018). However, little information exists in farmland buildings (Ogedegbe and Ogwu 2015), and thus, respect to the functions and structure of soil microorganisms in many research works have centered on the pest management termite mound soil. Termite mounds are the structures in sev- of termites. However, termites’ involvement as an agricultural eral tropical ecosystems that are primarily built by termites pest is merely trivial aspect as compared to the positive con- (Jouquet et al. 2015). Soil from termite mounds is rich in min- tributions of termites to agroecosystems. There are about 2600 eral nutrients and organic matter, and these make it a suitable taxonomically well-known species of termites, and of this habitat for microorganisms (Nithyatharani and Kavitha 2018). number, around 20% are destructive to agricultural crops Due to this nutrient richness of termite mound soil, small-scale (Sileshi et al. 2010;Deke etal. 2016). The guts of termites farmers often improve the soil condition of their farmland by contain numerous microscopic single-cell organisms of which using termite mound soil, which they believe can increase crop several are principally bacteria that can help in many metabol- yield (Deke et al. 2016). Microbial communities connected ic processes like decomposition of organic matter (Brune and with termite mounds play an important role in the maintenance Ohkuma 2010;Hongoh 2010). Previously, studies on the gut of the composition and fertility of soil through nitrogen fixa- ecosystem of termites concentrated on wood feeding termites, tion, acetogenesis, and lignocellulose breakdown, thus improv- for example, the study of Mathew et al. (2012)thatreported ing crop yield (Arumugam et al. 2016). Despite the contribu- thepresenceof Lactobacills, Peptococcus, Bacteriodetes, tions of termite mound bacteria in improving soil fertility, there Clostridium, Peptostreptococcus, Bifidobacterium, is little research involving the assessment of the bacterial rich- Ruminococcus, Fusobacterium, Eubacterium,and ness, abundance, and functional diversity in termite mound soil Termitomyces species (Bacteria that can break down cellulose) when compared to the assessment of the composition and func- in termites’ gut by using a gene-specific bacterial primer. tional diversity of bacteria in termite gut microbiota and the Termites build conspicuous structures called mounds in surrounding soil (Fall et al. 2007). Few researchers have used many humid ecosystems. They are constructed primarily by a cultivation-dependent and cultivation-independent (like the de- mixture of organic materials and clay components which is naturing gradient gel electrophoresis) tools to examine the glued by termites’ feces, saliva, and other secretions (Jouquet composition and abundance of bacteria in termite mound soil. et al. 2015). The mounds built by termites are solid as this makes it difficult for rain and predators to enter (Mujinya With the current trend in environmental microbiology, with the adoption of the high-throughput sequencing (HTS) approach to et al. 2013). The need of termite to normalize the temperature detect, identify, and monitor microorganisms in the environ- in their mound affects the shape of the mound and physico- ment, a comprehensive study of the bacterial diversity can chemical components of the soil and consequently leading to now be realized (Ercolini 2013). This HTS approach will help diverse biological habitats (Jouquet et al. 2015). Menichetti to reveal all the plant growth-promoting bacteria present in et al. (2014) stated that the daily activities of termites that feed termite mounds (Arumugam et al. 2016). This review is there- on litter is the key driving factor that circulates nutrients in soil fore aimed at assessing the potential of bacteria in termite occupied by them. This claim was backed by the studies on the mound soil to serve as biofertilizers and biocontrols as a prom- physicochemical properties of termite mound soil by ising tool for sustainable agriculture. Dhembare (2013) and Jouquet et al. (2015) that showed that organic carbon, pH, electric conductivity, magnesium, potassi- um, zinc, iron, phosphorus, copper, and clay content were in- Termite and termite mound soils creased in soil from termite mounds when compared with the corresponding neighboring soil. Another factor that can influ- Termites are a social insect that host a large amount of bacteria ence physicochemical properties of termite mound soil is the responsible for the breaking down of polyose and cellulose to parent soil type and this could also influence the shape of the a form that they can utilize (Bignell 2010). Termites are mounds, although not necessary the size (Jouquet et al. 2015). known to have a substantial effect on agroecosystems. They are referred to as Becosystem engineers^ as they can maintain, transform, and support soil fertility (Deke et al. 2016). Bacterial composition in termite mound soil Termites perform a significant contribution in upholding soil’s chemical and physical parameters by excavating and breaking Investigations into bacterial communities through various ap- down organic materials when constructing their mounds proaches like the use of metagenomics techniques (Fig. 1)have Ann Microbiol (2019) 69:211–219 213 Fig. 1 Metagenomics method, sequencing-based open-format technologies, data processing, and analysis for comprehensive in- vestigation of bacteria obtained from soil samples in termite mound shown the diverse nature of bacteria in termite mound soil mechanisms include direct solubilization of insoluble nutrients, (Manjula et al. 2014). Kumar et al. (2018) reported that the production of growth hormones, fixating of nitrogen (Fig. 2), bacteria population in both closed and open termite mound soil and through the production of lytic enzymes, siderophore, cy- are higher than in normal soil. This high diversity of bacteria in anides, fluorescent pigments, and antibiotics which help in termite mound soil could be as a result of the high amount of alienating soil pathogenic organisms capable of affecting plants organic matter in the termite mound. Several researchers have (Fig. 3)(Fuchsetal. 2001; Devi and Thakur 2018). reported the occurrence of Bacteroidetes, Firmicutes, Furthermore, these plants’ growth-promoting bacteria produce Spirochaetes, Chloroflexi, Nitrospirae, Planctomycetes, indole acetic acid that regulates cell divisions, elongation, and Proteobacteria, Tenericutes, Actinobacteria, Deinococcus- differentiation (Khare and Arora 2010). Devi and Thakur Thermus, SM2F11, Candidate division TM7, (2018) reported that during laboratory experiment, of the 70 Verrucomicrobia, Fibrobacteres, Chlorobi, Elusimicrobia, bacteria that belong to the genera Bacillus and Alcaligens iso- Candidate division WS3, Acidobacteria, Synergistetes, lated from termite mound soils 0.6–47.56 μg/mL of indole Cyanobacteria, WCHB1–60, Chlamydiae,and acetic acid was produced by 21 isolates, 9.27–65.48% SU of Gemmatimonadetes phyla in termite mound soil (Fall et al. siderophores produced by 12 isolates, while 13 isolates pro- 2007; Makonde et al. 2015; Manjula et al. 2016). Some strains duced ammonia in peptone broth and showed HCN production. of these bacterial phyla and their corresponding genes (Table 1) play a huge role in soil maintenance and this they do by hydro- lyzing lignocellulose materials, recycling nutrients, and fight- The role of bacteria in termite mound soil as biofertilizers ing against soil pathogens, which could increase crop yield (Manjula et al. 2016). From literature, it was observed that Soil fertility depends on the accessibility of stable nutrients in the type of termite that colonized the mound and the geograph- ical location of the mound influence the kind of bacteria present a form that plants can utilize (Gougoulias et al. 2014). The use of termite mound soil has been suggested as biofertilizers and in the termite mound soils (Table 2). inoculant in low-input cropping systems because it is rich in nutrients and plant growth-promoting bacteria (Dhembare and Underlying mechanism employed by some bacteria Pokale 2013; Menichetti et al. 2014;Deke etal. 2016). Local in termite mound soils in improving plant growth farmers in the plain areas of Laos and Northeast Thailand have started using termite mound soil for improving crop yield. Some bacteria such as Achromobacter, Agrobacterium, This is because of the high cost of chemical fertilizers Azotobacter, Bacillus, Burkholderia, Flavobacterium, (Miyagawa et al. 2011;Bhardwaj etal. 2014). In areas with Micrococcus, Pseudomonas,and Rhizobium with numerous limited amount of mineral fertilizers, there is a need to use plant growth-promoting activity isolated from termite mound some bacteria from termite mound soil to increase the avail- soils can support in tailoring of plant production as they insti- abilityof mineralsinsoil(Chauhanet al. 2017; Nithyatharani gate nutrient uptake, plant growth, and yield by a series of and Kavitha 2018). This idea could be crucial in sustaining mechanisms (Istina et al. 2015; Chakdar et al. 2018). These farming in such areas (Sánchez 2010). Termite mound soils 214 Ann Microbiol (2019) 69:211–219 Table 1 Role of termite mound soil bacteria in improving soil fertility and plant growth Bacteria Mound Effect on soil, crop growth, and pathogen References Fluorescent pseudomonads Macrotermes subhyalinus The inoculation of Fluorescent pseudomonads Duponnois et al. (2006)) to sorghum plants significantly improved the shoot and total biomass of sorghum plants when compared to the control Bacillus endophyticus TSH42 Termitarium They increased turmeric plant growth and Chauhan et al. (2017)) and Bacillus cereus TSH77 production up to 18% in field trial when bacterized individually and in combined form in comparison to non-bacterized plants Flavobacterium Odontotermes obesus They have denitrification genes and carry out Sarkar (1991)) denitrification in soil Thiobacillus and Rhizobium Termitarium They aid in nitrogen fixation therefore Manjula et al. (2014)) enhancing soil fertility Chlorobi Macrotermes natalensis, They oxidize and reduce sulfur compounds Makonde et al. (2015)) Microtermes sp., and for CO fixation via the reverse Odontotermes sp. tricarboxylic acid cycle and can perform N fixation Planctomycetes Cornitermes cumulans They oxidize ammonia to dinitrogen without Costa et al. (2013)) oxygen and play a major part in nitrogen cycle Chloroflexi Cubitermes niokoloensis Their corresponding nifH genes are significant Fall et al. (2007)) nitrogen fixer have been reported to contain phosphate-solubilizing bacteria (IAA), solubilization of phosphate, and production of population which through the production of organic acids, siderophore by the bacteria. It is of importance to note that chelation and exchange reactions can mobilize vital nutritional termite mound soils hold higher amount of phosphorus when elements in the soil by hydrolyzing both inorganic and organic compared to the surrounding soils (López-Hernández 2001). phosphorus from soluble compounds (Chakdar et al. 2018). This is because of the highly efficient phosphate-solubilizing The ability of these phosphate-solubilizing bacteria to solubi- bacteria present in termite mound soils (Chakdar et al. 2018). lize inorganic and organic phosphorus is seen as a significant Pseudomonas fluorescens—a well-known phosphate-solubi- feature for increasing soil fertility and their use as an inoculant lizing bacteria, was reported to dissolve rock phosphate in an concurrently increases plant P uptake and increase crop yield experiment where termite mound soil were used as microbial (Bama and Ravindran 2012). 2-Keto gluconic acid and inoculum to support Acacia seyal growth. From the result, it gluconic acid (major organic acids for solubilization of phos- was observed that the leaves, height, and shoot biomass of phate) were produced by Kosakonia, Bacillus,and Pantoea Acacia seyal were better developed in the soil where termite isolated from termite mound soils (Chakdar et al. 2018). From mound soils were used as inoculant. They then concluded that an experiment, it was shown that after 24 h of incubation, termite mound soil could stimulate the growth of bacterial strains of Pantoea isolated from termite mound soils solubi- populations that can break down materials essential for plant lized tri-calcium phosphate to the tune of 1067.33 mg/L growth (Duponnois et al. 2005). (while comparing it with the strains of Pantoea isolated from Several researchers have identified bacteria phyla which soils of Western Ghat forest, it only solubilized tri-calcium are nitrogen fixers such as the Chloroflexi, Cyanobacteria, phosphate to the tune of 28 mg/L) (Dastager et al. 2009; and Proteobacteria in termite mound soil (Ntambo et al. Chakdar et al. 2018). Furthermore, when seeds were bacte- 2010; Makonde et al. 2015;Arumugametal. 2016; Manjula rized with Pantoea sp. A3 and Kosakonia sp. A37, it resulted et al. 2016). Strains of these phyla such as symbiotic in ~37% and ~53% increase in root length of tomato seed- diazotrophic bacteria belonging to Chloroflexaceae, lings, respectively (Chakdar et al. 2018). Bacillus cereus Methylocystaceae, Pseudomonadaceae, Enterobacteriaceae, TSH77 and Bacillus endophyticus TSH42 isolated from ter- and their corresponding nifH genes are significant nitrogen mite mound soils were used to bacterize the rhizome of fixers (Da Silva Fonseca et al. 2018). Nithyatharani and Curcuma longa. Both strains showed remarkable plant Kavitha (2018) successfully isolated four different bacteria growth-promoting (PGP) activities. This led to an increase species from termite mound soil and these bacteria contribute in Curcuma longa growth and production by 18% when com- to soil fertility. They include Citrobacter fruendii, anitrogen pared with non-bacterize Curcuma longa (Chauhan et al. fixer; Enterobacter sp. which contribute to acetogenesis; 2017). This increase in plant growth and rhizome biomass Paenibacillus sp. which are capable of reducing sulfur mole- was owned to the high production of the indole acetic acid cules to a form which plants can utilize to enhance metabolism Ann Microbiol (2019) 69:211–219 215 Table 2 Bacteria reported present in termite mound soils and their corresponding surrounding soils Country Termite type Bacteria present in termite mound soil Bacteria present in surrounding soil Reference Kenya Macrotermes michaelseni Proteobacteria, Nitrospirae, Armatimonadetes, SM2F11, WCHB1–60 Makonde et al. (2015)) Gemmatimonadetes, Firmicutes, Spirochaetes, Proteobacteria, Fibrobacteres, Cyanobacteria, Planctomycetes, Nitrospirae, Chloroflexi, Bacteroidetes, Gemmatimonadetes, Firmicutes, Acidobacteria,and Actinobacteria Fibrobacteres, Elusimicrobia, Cyanobacteria, Chloroflexi, Chlorobi, Candidate division WS3, Bacteroidetes, Acidobacteria,and Actinobacteria Kenya Odontotermes sp. Candidate division, TM7, Armatimonadetes, SM2F11, Makonde et al. (2015)) Bacteroidetes, Chlorobi, WCHB1–60 Spirochaetes, Proteobacteria, Candidate division WS3, Planctomycetes, Nitrospirae, Acidobacteria, Actinobacteria, Gemmatimonadetes, Firmicutes, Elusimicrobia, Planctomycetes, Fibrobacteres, Elusimicrobia, Spirochaetes Cyanobacteria, Chloroflexi, Chlorobi, Candidate division WS3, Bacteroidetes, Acidobacteria,and Actinobacteria Senegal Cubitermes niokoloensis Firmicutes, Actinobacteria, Firmicutes, Alphaproteobacteria, Fall et al. (2007)) Chloroflexi,and Planctomycetes Bacteroidetes, Chlorobi, Deltaproteobacteria,and Chloroflexi India Not specified Actinobacteria, Firmicutes, – Manjula et al. (2014)) Chlorobi, Synergistetes, Bacteroidetes, Cyanobacteria, Deinococcus-Thermus, Proteobacteria,and Spirochaetes India Not specified Nitrospirae, Chloroflexi, – Manjula et al. (2016)) Bacteroidetes, Gemmatimonadetes, Tenericutes, Actinobacteria, Fibrobacteres, Deinococcus, Planctomycetes, Firmicutes, Chlamydiae, Proteobacteria, Acidobacteria,and Verrucomicrobia Thailand Not specified Streptomyces, Amycolatopsis, – Sujada et al. (2014)) Pseudonocardia, Micromonospora, and Nocardia and growth; and Lactococcus sp. Reasonable numbers of bac- improved the porosity and transformed the pore size distribu- teria strains which exist in termite mound soil are capable of tion causing an increase in the obtainable water content for crop breaking down plant biomass polysaccharides (Koeck et al. growth (Suzuki et al. 2007). The combined use of 200 g of 2014; Nithyatharani and Kavitha 2018), and they are also able termite mound material with NPK fertilizer led to a substantial to break down lignin and phenolic compounds (Bandounas increase in Solatium melongena production (Batalha et al. et al. 2011). Paul and Varma (1993) and Sexana et al. (1993) 1995). Watson (1977) planted perennial ryegrass on termite reported the occurrence of Bacillus and Cellulomonas sp. in mound soil in pot experiments and reported that perennial rye- termite mound soil, and these bacteria are known for grass gave higher dry-matter yields with substrates derived decomposing cellulose and xylan. from termite mound than the comparable soil. He then conclud- Termite mound soil was used as a soil amendment by Garba ed that crop production can be increased by augmenting soil et al. (2011) in an attempt to evaluate the influence of termite with termite mound materials. mound soil on sandy soil physical parameters and on the growth characteristics of Solanum lycopersicum L. Their find- The role of bacteria in termite mound soil ings showed that soil mixed with termite mound material had as biocontrol larger clay size particles and higher organic carbon content than unamended soil. Furthermore, Solanum lycopersicum L. Plant rhizosphere is a very competitive region and occupied plantedinamendedsoil hadbetter plant height, an increase in by many microorganisms because of the high nutrient avail- leaf number, fruits, and drymatterwhencomparedto Solanum ability extruded by mucilage and roots of plants (Chowdhury lycopersicum L. grown on unamended soil. Combining sandy et al. 2015). The living and non-living factors in rhizosphere soil with termite mound materials at a proportion of 120 mg/ha influence the growth of agricultural plants (Igiehon and 216 Ann Microbiol (2019) 69:211–219 Fig. 2 Potiential use of bacteria in termite mound soil as biofertilizer in improving crop yield Babalola 2018). Plants respond to their environment through apoplastic exudation molecules of low molecular weight in their hormones like ethylene, gibberellin, cytokines, auxins, Arabidopsis thaliana. This they do by the introduction of in- and abscisic acid (Alori et al. 2017). Some bacteria in the duced systemic resistance; thus, an immune signaling force is rhizosphere known as plant growth-promoting rhizobacteria instigated systemically against a broad spectrum of disease- influence the physiology of the plant to a large extent (Alori causing organisms (Millet et al. 2010; Berendsen et al. 2012). et al. 2017), and they can suppress soil borne plant pathogens Plant pathogens pose a prolonged threat to food production through the stimulation of plant-induced systemic resistance at a global scale (Devi et al. 2018). Synthetic agrochemicals and the production of nematicidal, antiviral, and antimicrobial are frequently used in protecting plants from disease-causing substances (Doornbos et al. 2012). Plant growth-promoting organisms. However, unselective application of the synthetic bacteria are able to suppress pathogenic organisms by using agrochemicals can cause numerous adverse effects on human the mechanism (Fig. 3) of producing siderophore, lytic en- and environmental health (Mahdi et al. 2010). Recently, mi- zymes, antibiotics, fluorescent pigments, and cyanides crobial inoculants have been used as an ecologically friendly (Babalola 2010; Olanrewaju et al. 2017) or by consuming approach in suppressing or fighting plant pathogens (Ayitso compounds which stimulate the pathogens and competing et al. 2015). Termite mound material is seen as an ecologically with the pathogens for nutrients (Berg 2009; Doornbos et al. friendly method for reducing inorganic fertilizers through bi- 2012). For instance, Pseudomonas fluorescens WCS417 sup- ological activities, as they are loaded with microorganisms press flagellin triggered by immune responses through capable of suppressing soil borne plant pathogens and Fig. 3 Mechanisms used by plant growth-promoting bacteria to suppress plant pathogenic organisms Ann Microbiol (2019) 69:211–219 217 Publisher’snote Springer Nature remains neutral with regard to jurisdic- mobilizing vital nutritional elements in soil (Bama and tional claims in published maps and institutional affiliations. Ravindran 2012; Devi et al. 2018). Chauhan et al. (2016) reported that B. endophyticus TSH42 and B. cereus TSH77 isolated from termite mound soil significantly slow down the References growth of Fusarium solani (a plant pathogen causing rot dis- ease in crops like potato). Investigation of the acidified cell- Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubi- free culture filtrate using liquid chromatography–mass spec- lization and its potential for use in sustainable agriculture. Front trometry showed that B. cereus TSH77 are made up of Microbiol 8:971 Arumugam M, Pushpanathan M, Sathyavathi S, Gunasekaran P, fengycin and surfactin while B. endophyticus TSH42 Rajendhran J (2016) Comparative analysis of microbial diversity contained fengycin, surfactin, and iturin. The rhizome rot dis- in termite gut and termite nest using ion sequencing. Curr eases in Curcuma longa L. were controlled, when treated with Microbiol 72:267–275 three strains of these bacteria. Staphylococcus saprophyticus Ayitso AS, Onyango DM, Wagai SO (2015) Antimicrobial activities of microorganisms obtained from the gut of Macrotermes michaelseni and Bacillus methylotrophicus isolated from termite mound in Maseno, Kenya. J Appl Biol Biotechnol 3(06):048–052 also showed antifungal activity against Fusarium oxysporum, Babalola OO (2010) Beneficial bacteria of agricultural importance. Alternaria brassicae, Rhizoctonia solani, Sclerotium rolfsii, Biotechnol Lett 32(11):1559–1570 and Colletotrichum truncatum (Devietal. 2018). Bama PS, Ravindran AD (2012) Dynamics of P sorption and solubilising Antimicrobial activity of Streptomyces sp. isolated from the activity in termite nest material. Asian J Res Soc Sci Hum 2(10): 231–237 termite mound material was tested against Metarhizium Bandounas L, Wierckx NJ, De Winde JH, Ruijssenaars HJ (2011) anisopliae (a fungal entomopathogen), and the occurrence of Isolation and characterization of novel bacterial strains exhibiting Streptomyces within the mound structure offered a substantial ligninolytic potential. 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Microb Cell Factories that quest without compromising the safety of the environ- 13(1):66 ment or human health. As a result of the grave health and Bignell DE (2010) Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland biology of environmental problems associated with the use of chemical termites: a modern synthesis. Springer, Dordrecht, pp 375–412 fertilizers and pesticides globally, there is a need for alterna- Brune A, Ohkuma M (2010) Role of the termite gut microbiota in sym- tive safe measures. Termite mound soil contains useful bacte- biotic digestion biology of termites: a modern synthesis. Springer, ria that are capable of decomposing lignin and cellulose, fix- Dordrecht, pp 439–475 ing nitrogen, solubilizing phosphate, and suppressing plant Chakdar H, Dastager SG, Khire JM, Rane D, Dharne MS (2018) Characterization of mineral phosphate solubilizing and plant growth soil pathogens. These have put them in a position to function promoting bacteria from termite soil of arid region. Biotech 8(11): as biofertilizers and biocontrol. For the future success of ter- 463. https://doi.org/10.1007/s13205-018-1488-4 mite mound soil usage as biofertilizers and biocontrol, exten- Chauhan AK, Maheshwari DK, Kim K, Bajpai VK (2016) Termitarium- sive research is still required to unveil their full potential. inhabiting Bacillus endophyticus TSH42 and Bacillus cereus TSH77 colonizing Curcuma longa L.: isolation, characterization, and evaluation of their biocontrol and plant-growth-promoting ac- Author contributions B.J.E. wrote the first draft. O.O.B. provided the tivities. Can J Microbiol 62(10):880–892 academic input and thoroughly critiqued the article. Both authors ap- Chauhan AK, Maheshwari DK, Dheeman S, Bajpai VK (2017) proved the article for publication. Termitarium-inhabiting Bacillus spp. enhanced plant growth and bioactive component in turmeric (Curcuma longa L.). Curr Funding Information Support to B.J.E.’s Doctoral program was provid- Microbiol 74(2):184–192 ed by the South Africa’s National Research Foundation/The World Choudhary M, Datta A, Jat HS et al (2018) Changes in soil biology under Academy of Science African Renaissance grant (UID110909). The conservation agriculture based sustainable intensification of cereal National Research Foundation, South Africa for the grant (UID81192) systems in indo-Gangetic Plains. Geoderma 313:193–204 provided support to O.O.B. that has supported research in her lab. Chouvenc T, Efstathion CA, Elliott ML, Su N-Y (2013) Extended disease resistance emerging from the faecal nest of a subterranean termite. Compliance with ethical standards Proc R Soc Biol Sci 280(1770):1–9 Chowdhury SP, Hartmann A, Gao X, Borriss R (2015) Biocontrol mech- anism by root-associated Bacillus amyloliquefaciens FZB42–are- Conflict of interest The authors declare that they have no conflict of view. 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Potentials of termite mound soil bacteria in ecosystem engineering for sustainable agriculture

Annals of Microbiology , Volume 69 (3) – Jan 30, 2019

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References (72)

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Springer Journals
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Copyright © 2019 by Università degli studi di Milano
Subject
Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Mycology; Medical Microbiology; Applied Microbiology
ISSN
1590-4261
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1869-2044
DOI
10.1007/s13213-019-1439-2
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Abstract

The environmental deteriorating effects arising from the misuse of pesticides and chemical fertilizers in agriculture has resulted in the pursuit of eco-friendly means of producing agricultural produce without compromising the safety of the environment. Thus, the purpose of this review is to assess the potential of bacteria in termite mound soil to serve as biofertilizer and biocontrol as a promising tool for sustainable agriculture. This review has been divided into four main sections: termite and termite mound soils, bacterial composition in termite mound soil, the role of bacteria in termite mound soil as biofertilizers, and the role of bacteria in termite mound soil as biocontrol. Some bacteria in termite mound soils have been isolated and characterized by various means, and these bacteria could improve the fertility of the soil and suppress soil borne plant pathogens through the production of antibiotics, nutrient fixation, and other means. These bacteria in termite mound soils could serve as a remarkable means of reducing the reliance on the usage of chemical fertilizers and pesticides in farming, thereby increasing crop yield. . . . . Keywords Biofertilizers Chemical fertilizers Environmental safety Food security Organic farming Introduction which will certainly increase as human population increases, it is therefore paramount to produce agricultural produce in a sus- tainable manner without causing any harm to the environment Traditional agriculture contributes a key part in meeting the demand for food of a rising human populations (Santos et al. (Pathak et al. 2018). To achieve this, eco-friendly methods like 2012) that is currently more than seven billion people globally, the use of biofertilizers and biocontrols need to be employed to and this figure is expected to rise to eight billion by 2020 boost soil fertility and suppress soil plant pathogens (Igiehon (Conway 2012). The use of pesticides and inorganic fertilizers and Babalola 2017). Biofertilizers are substances that are made to boost the fertility of soil and control plant pests has increased up of live microorganisms (which could be plant growth- food production; however, their misuse has resulted in eutrophi- promoting rhizobacteria (PGPR)) which when applied to soil, cation of water bodies, air, and groundwater pollution, thus plant, or seeds, inhabit the rhizosphere of plants and stimulate affecting human and environmental health (Savci 2012;Alori plant growth (Malusá and Vassilev 2014). PGPR enrich the soil et al. 2017). The prolonged use of these chemicals affects soil by through potassium solubilization, phosphate mineralization, and reducing its water-holding capacity, increasing soil salt content, nitrogen fixation, breaking down organic substances to a form leading to inequality of soil nutrient distribution, and ultimately that plants can utilize. Further, they help in the regulation of affecting the structure and fertility of soil (Savci 2012). Looking plant growth substances and the production of antibiotics that at these negative effects of chemical fertilizers and pesticides, suppress soil borne plant pathogens (they are microscopic or- ganisms that prefer to live within the soil causing harm to plants and even soil itself) such as virus, bacterium, fungus, or nema- * Olubukola Oluranti Babalola tode (Liu et al. 2018; Parewa et al. 2018) that cause damaging olubukola.babalola@nwu.ac.za effects on fruits and growing and stored crops of economic Ben Jesuorsemwen Enagbonma importance, therefore leading to plant diseases which contribute enagbonma30@yahoo.com directly to losses in agriculture (Widmer 2014). Investigations associated with soil uniqueness in controlling Food Security and Safety Niche, Faculty of Natural and Agricultural soil microbial community composition could enlighten our un- Sciences, North-West University, Private Mail Bag X2046, derstanding of soil quality and biogeochemical processes (Li Mmabatho 2735, South Africa 212 Ann Microbiol (2019) 69:211–219 et al. 2015). The structures and functions of soil microorgan- (Jouquet et al. 2015; Vidyashree et al. 2018). Termites feed isms are widely used as a pointer to assess the degree of soil on plant materials, fungi, and humus, and because of their health (Zhu et al. 2017). This is because soil microorganisms feeding habit, they are considered as a big menace to agricul- function as a means of transforming carbon-based materials, tural produce in sub-tropical and tropical areas (Rosengaus cycling minerals, and energy and also perform further roles that et al. 2011; Negassa and Sileshi 2018). This is because they could advance soil health and agricultural sustainability have the tendency of destroying growing or stored crops and (Choudhary et al. 2018). However, little information exists in farmland buildings (Ogedegbe and Ogwu 2015), and thus, respect to the functions and structure of soil microorganisms in many research works have centered on the pest management termite mound soil. Termite mounds are the structures in sev- of termites. However, termites’ involvement as an agricultural eral tropical ecosystems that are primarily built by termites pest is merely trivial aspect as compared to the positive con- (Jouquet et al. 2015). Soil from termite mounds is rich in min- tributions of termites to agroecosystems. There are about 2600 eral nutrients and organic matter, and these make it a suitable taxonomically well-known species of termites, and of this habitat for microorganisms (Nithyatharani and Kavitha 2018). number, around 20% are destructive to agricultural crops Due to this nutrient richness of termite mound soil, small-scale (Sileshi et al. 2010;Deke etal. 2016). The guts of termites farmers often improve the soil condition of their farmland by contain numerous microscopic single-cell organisms of which using termite mound soil, which they believe can increase crop several are principally bacteria that can help in many metabol- yield (Deke et al. 2016). Microbial communities connected ic processes like decomposition of organic matter (Brune and with termite mounds play an important role in the maintenance Ohkuma 2010;Hongoh 2010). Previously, studies on the gut of the composition and fertility of soil through nitrogen fixa- ecosystem of termites concentrated on wood feeding termites, tion, acetogenesis, and lignocellulose breakdown, thus improv- for example, the study of Mathew et al. (2012)thatreported ing crop yield (Arumugam et al. 2016). Despite the contribu- thepresenceof Lactobacills, Peptococcus, Bacteriodetes, tions of termite mound bacteria in improving soil fertility, there Clostridium, Peptostreptococcus, Bifidobacterium, is little research involving the assessment of the bacterial rich- Ruminococcus, Fusobacterium, Eubacterium,and ness, abundance, and functional diversity in termite mound soil Termitomyces species (Bacteria that can break down cellulose) when compared to the assessment of the composition and func- in termites’ gut by using a gene-specific bacterial primer. tional diversity of bacteria in termite gut microbiota and the Termites build conspicuous structures called mounds in surrounding soil (Fall et al. 2007). Few researchers have used many humid ecosystems. They are constructed primarily by a cultivation-dependent and cultivation-independent (like the de- mixture of organic materials and clay components which is naturing gradient gel electrophoresis) tools to examine the glued by termites’ feces, saliva, and other secretions (Jouquet composition and abundance of bacteria in termite mound soil. et al. 2015). The mounds built by termites are solid as this makes it difficult for rain and predators to enter (Mujinya With the current trend in environmental microbiology, with the adoption of the high-throughput sequencing (HTS) approach to et al. 2013). The need of termite to normalize the temperature detect, identify, and monitor microorganisms in the environ- in their mound affects the shape of the mound and physico- ment, a comprehensive study of the bacterial diversity can chemical components of the soil and consequently leading to now be realized (Ercolini 2013). This HTS approach will help diverse biological habitats (Jouquet et al. 2015). Menichetti to reveal all the plant growth-promoting bacteria present in et al. (2014) stated that the daily activities of termites that feed termite mounds (Arumugam et al. 2016). This review is there- on litter is the key driving factor that circulates nutrients in soil fore aimed at assessing the potential of bacteria in termite occupied by them. This claim was backed by the studies on the mound soil to serve as biofertilizers and biocontrols as a prom- physicochemical properties of termite mound soil by ising tool for sustainable agriculture. Dhembare (2013) and Jouquet et al. (2015) that showed that organic carbon, pH, electric conductivity, magnesium, potassi- um, zinc, iron, phosphorus, copper, and clay content were in- Termite and termite mound soils creased in soil from termite mounds when compared with the corresponding neighboring soil. Another factor that can influ- Termites are a social insect that host a large amount of bacteria ence physicochemical properties of termite mound soil is the responsible for the breaking down of polyose and cellulose to parent soil type and this could also influence the shape of the a form that they can utilize (Bignell 2010). Termites are mounds, although not necessary the size (Jouquet et al. 2015). known to have a substantial effect on agroecosystems. They are referred to as Becosystem engineers^ as they can maintain, transform, and support soil fertility (Deke et al. 2016). Bacterial composition in termite mound soil Termites perform a significant contribution in upholding soil’s chemical and physical parameters by excavating and breaking Investigations into bacterial communities through various ap- down organic materials when constructing their mounds proaches like the use of metagenomics techniques (Fig. 1)have Ann Microbiol (2019) 69:211–219 213 Fig. 1 Metagenomics method, sequencing-based open-format technologies, data processing, and analysis for comprehensive in- vestigation of bacteria obtained from soil samples in termite mound shown the diverse nature of bacteria in termite mound soil mechanisms include direct solubilization of insoluble nutrients, (Manjula et al. 2014). Kumar et al. (2018) reported that the production of growth hormones, fixating of nitrogen (Fig. 2), bacteria population in both closed and open termite mound soil and through the production of lytic enzymes, siderophore, cy- are higher than in normal soil. This high diversity of bacteria in anides, fluorescent pigments, and antibiotics which help in termite mound soil could be as a result of the high amount of alienating soil pathogenic organisms capable of affecting plants organic matter in the termite mound. Several researchers have (Fig. 3)(Fuchsetal. 2001; Devi and Thakur 2018). reported the occurrence of Bacteroidetes, Firmicutes, Furthermore, these plants’ growth-promoting bacteria produce Spirochaetes, Chloroflexi, Nitrospirae, Planctomycetes, indole acetic acid that regulates cell divisions, elongation, and Proteobacteria, Tenericutes, Actinobacteria, Deinococcus- differentiation (Khare and Arora 2010). Devi and Thakur Thermus, SM2F11, Candidate division TM7, (2018) reported that during laboratory experiment, of the 70 Verrucomicrobia, Fibrobacteres, Chlorobi, Elusimicrobia, bacteria that belong to the genera Bacillus and Alcaligens iso- Candidate division WS3, Acidobacteria, Synergistetes, lated from termite mound soils 0.6–47.56 μg/mL of indole Cyanobacteria, WCHB1–60, Chlamydiae,and acetic acid was produced by 21 isolates, 9.27–65.48% SU of Gemmatimonadetes phyla in termite mound soil (Fall et al. siderophores produced by 12 isolates, while 13 isolates pro- 2007; Makonde et al. 2015; Manjula et al. 2016). Some strains duced ammonia in peptone broth and showed HCN production. of these bacterial phyla and their corresponding genes (Table 1) play a huge role in soil maintenance and this they do by hydro- lyzing lignocellulose materials, recycling nutrients, and fight- The role of bacteria in termite mound soil as biofertilizers ing against soil pathogens, which could increase crop yield (Manjula et al. 2016). From literature, it was observed that Soil fertility depends on the accessibility of stable nutrients in the type of termite that colonized the mound and the geograph- ical location of the mound influence the kind of bacteria present a form that plants can utilize (Gougoulias et al. 2014). The use of termite mound soil has been suggested as biofertilizers and in the termite mound soils (Table 2). inoculant in low-input cropping systems because it is rich in nutrients and plant growth-promoting bacteria (Dhembare and Underlying mechanism employed by some bacteria Pokale 2013; Menichetti et al. 2014;Deke etal. 2016). Local in termite mound soils in improving plant growth farmers in the plain areas of Laos and Northeast Thailand have started using termite mound soil for improving crop yield. Some bacteria such as Achromobacter, Agrobacterium, This is because of the high cost of chemical fertilizers Azotobacter, Bacillus, Burkholderia, Flavobacterium, (Miyagawa et al. 2011;Bhardwaj etal. 2014). In areas with Micrococcus, Pseudomonas,and Rhizobium with numerous limited amount of mineral fertilizers, there is a need to use plant growth-promoting activity isolated from termite mound some bacteria from termite mound soil to increase the avail- soils can support in tailoring of plant production as they insti- abilityof mineralsinsoil(Chauhanet al. 2017; Nithyatharani gate nutrient uptake, plant growth, and yield by a series of and Kavitha 2018). This idea could be crucial in sustaining mechanisms (Istina et al. 2015; Chakdar et al. 2018). These farming in such areas (Sánchez 2010). Termite mound soils 214 Ann Microbiol (2019) 69:211–219 Table 1 Role of termite mound soil bacteria in improving soil fertility and plant growth Bacteria Mound Effect on soil, crop growth, and pathogen References Fluorescent pseudomonads Macrotermes subhyalinus The inoculation of Fluorescent pseudomonads Duponnois et al. (2006)) to sorghum plants significantly improved the shoot and total biomass of sorghum plants when compared to the control Bacillus endophyticus TSH42 Termitarium They increased turmeric plant growth and Chauhan et al. (2017)) and Bacillus cereus TSH77 production up to 18% in field trial when bacterized individually and in combined form in comparison to non-bacterized plants Flavobacterium Odontotermes obesus They have denitrification genes and carry out Sarkar (1991)) denitrification in soil Thiobacillus and Rhizobium Termitarium They aid in nitrogen fixation therefore Manjula et al. (2014)) enhancing soil fertility Chlorobi Macrotermes natalensis, They oxidize and reduce sulfur compounds Makonde et al. (2015)) Microtermes sp., and for CO fixation via the reverse Odontotermes sp. tricarboxylic acid cycle and can perform N fixation Planctomycetes Cornitermes cumulans They oxidize ammonia to dinitrogen without Costa et al. (2013)) oxygen and play a major part in nitrogen cycle Chloroflexi Cubitermes niokoloensis Their corresponding nifH genes are significant Fall et al. (2007)) nitrogen fixer have been reported to contain phosphate-solubilizing bacteria (IAA), solubilization of phosphate, and production of population which through the production of organic acids, siderophore by the bacteria. It is of importance to note that chelation and exchange reactions can mobilize vital nutritional termite mound soils hold higher amount of phosphorus when elements in the soil by hydrolyzing both inorganic and organic compared to the surrounding soils (López-Hernández 2001). phosphorus from soluble compounds (Chakdar et al. 2018). This is because of the highly efficient phosphate-solubilizing The ability of these phosphate-solubilizing bacteria to solubi- bacteria present in termite mound soils (Chakdar et al. 2018). lize inorganic and organic phosphorus is seen as a significant Pseudomonas fluorescens—a well-known phosphate-solubi- feature for increasing soil fertility and their use as an inoculant lizing bacteria, was reported to dissolve rock phosphate in an concurrently increases plant P uptake and increase crop yield experiment where termite mound soil were used as microbial (Bama and Ravindran 2012). 2-Keto gluconic acid and inoculum to support Acacia seyal growth. From the result, it gluconic acid (major organic acids for solubilization of phos- was observed that the leaves, height, and shoot biomass of phate) were produced by Kosakonia, Bacillus,and Pantoea Acacia seyal were better developed in the soil where termite isolated from termite mound soils (Chakdar et al. 2018). From mound soils were used as inoculant. They then concluded that an experiment, it was shown that after 24 h of incubation, termite mound soil could stimulate the growth of bacterial strains of Pantoea isolated from termite mound soils solubi- populations that can break down materials essential for plant lized tri-calcium phosphate to the tune of 1067.33 mg/L growth (Duponnois et al. 2005). (while comparing it with the strains of Pantoea isolated from Several researchers have identified bacteria phyla which soils of Western Ghat forest, it only solubilized tri-calcium are nitrogen fixers such as the Chloroflexi, Cyanobacteria, phosphate to the tune of 28 mg/L) (Dastager et al. 2009; and Proteobacteria in termite mound soil (Ntambo et al. Chakdar et al. 2018). Furthermore, when seeds were bacte- 2010; Makonde et al. 2015;Arumugametal. 2016; Manjula rized with Pantoea sp. A3 and Kosakonia sp. A37, it resulted et al. 2016). Strains of these phyla such as symbiotic in ~37% and ~53% increase in root length of tomato seed- diazotrophic bacteria belonging to Chloroflexaceae, lings, respectively (Chakdar et al. 2018). Bacillus cereus Methylocystaceae, Pseudomonadaceae, Enterobacteriaceae, TSH77 and Bacillus endophyticus TSH42 isolated from ter- and their corresponding nifH genes are significant nitrogen mite mound soils were used to bacterize the rhizome of fixers (Da Silva Fonseca et al. 2018). Nithyatharani and Curcuma longa. Both strains showed remarkable plant Kavitha (2018) successfully isolated four different bacteria growth-promoting (PGP) activities. This led to an increase species from termite mound soil and these bacteria contribute in Curcuma longa growth and production by 18% when com- to soil fertility. They include Citrobacter fruendii, anitrogen pared with non-bacterize Curcuma longa (Chauhan et al. fixer; Enterobacter sp. which contribute to acetogenesis; 2017). This increase in plant growth and rhizome biomass Paenibacillus sp. which are capable of reducing sulfur mole- was owned to the high production of the indole acetic acid cules to a form which plants can utilize to enhance metabolism Ann Microbiol (2019) 69:211–219 215 Table 2 Bacteria reported present in termite mound soils and their corresponding surrounding soils Country Termite type Bacteria present in termite mound soil Bacteria present in surrounding soil Reference Kenya Macrotermes michaelseni Proteobacteria, Nitrospirae, Armatimonadetes, SM2F11, WCHB1–60 Makonde et al. (2015)) Gemmatimonadetes, Firmicutes, Spirochaetes, Proteobacteria, Fibrobacteres, Cyanobacteria, Planctomycetes, Nitrospirae, Chloroflexi, Bacteroidetes, Gemmatimonadetes, Firmicutes, Acidobacteria,and Actinobacteria Fibrobacteres, Elusimicrobia, Cyanobacteria, Chloroflexi, Chlorobi, Candidate division WS3, Bacteroidetes, Acidobacteria,and Actinobacteria Kenya Odontotermes sp. Candidate division, TM7, Armatimonadetes, SM2F11, Makonde et al. (2015)) Bacteroidetes, Chlorobi, WCHB1–60 Spirochaetes, Proteobacteria, Candidate division WS3, Planctomycetes, Nitrospirae, Acidobacteria, Actinobacteria, Gemmatimonadetes, Firmicutes, Elusimicrobia, Planctomycetes, Fibrobacteres, Elusimicrobia, Spirochaetes Cyanobacteria, Chloroflexi, Chlorobi, Candidate division WS3, Bacteroidetes, Acidobacteria,and Actinobacteria Senegal Cubitermes niokoloensis Firmicutes, Actinobacteria, Firmicutes, Alphaproteobacteria, Fall et al. (2007)) Chloroflexi,and Planctomycetes Bacteroidetes, Chlorobi, Deltaproteobacteria,and Chloroflexi India Not specified Actinobacteria, Firmicutes, – Manjula et al. (2014)) Chlorobi, Synergistetes, Bacteroidetes, Cyanobacteria, Deinococcus-Thermus, Proteobacteria,and Spirochaetes India Not specified Nitrospirae, Chloroflexi, – Manjula et al. (2016)) Bacteroidetes, Gemmatimonadetes, Tenericutes, Actinobacteria, Fibrobacteres, Deinococcus, Planctomycetes, Firmicutes, Chlamydiae, Proteobacteria, Acidobacteria,and Verrucomicrobia Thailand Not specified Streptomyces, Amycolatopsis, – Sujada et al. (2014)) Pseudonocardia, Micromonospora, and Nocardia and growth; and Lactococcus sp. Reasonable numbers of bac- improved the porosity and transformed the pore size distribu- teria strains which exist in termite mound soil are capable of tion causing an increase in the obtainable water content for crop breaking down plant biomass polysaccharides (Koeck et al. growth (Suzuki et al. 2007). The combined use of 200 g of 2014; Nithyatharani and Kavitha 2018), and they are also able termite mound material with NPK fertilizer led to a substantial to break down lignin and phenolic compounds (Bandounas increase in Solatium melongena production (Batalha et al. et al. 2011). Paul and Varma (1993) and Sexana et al. (1993) 1995). Watson (1977) planted perennial ryegrass on termite reported the occurrence of Bacillus and Cellulomonas sp. in mound soil in pot experiments and reported that perennial rye- termite mound soil, and these bacteria are known for grass gave higher dry-matter yields with substrates derived decomposing cellulose and xylan. from termite mound than the comparable soil. He then conclud- Termite mound soil was used as a soil amendment by Garba ed that crop production can be increased by augmenting soil et al. (2011) in an attempt to evaluate the influence of termite with termite mound materials. mound soil on sandy soil physical parameters and on the growth characteristics of Solanum lycopersicum L. Their find- The role of bacteria in termite mound soil ings showed that soil mixed with termite mound material had as biocontrol larger clay size particles and higher organic carbon content than unamended soil. Furthermore, Solanum lycopersicum L. Plant rhizosphere is a very competitive region and occupied plantedinamendedsoil hadbetter plant height, an increase in by many microorganisms because of the high nutrient avail- leaf number, fruits, and drymatterwhencomparedto Solanum ability extruded by mucilage and roots of plants (Chowdhury lycopersicum L. grown on unamended soil. Combining sandy et al. 2015). The living and non-living factors in rhizosphere soil with termite mound materials at a proportion of 120 mg/ha influence the growth of agricultural plants (Igiehon and 216 Ann Microbiol (2019) 69:211–219 Fig. 2 Potiential use of bacteria in termite mound soil as biofertilizer in improving crop yield Babalola 2018). Plants respond to their environment through apoplastic exudation molecules of low molecular weight in their hormones like ethylene, gibberellin, cytokines, auxins, Arabidopsis thaliana. This they do by the introduction of in- and abscisic acid (Alori et al. 2017). Some bacteria in the duced systemic resistance; thus, an immune signaling force is rhizosphere known as plant growth-promoting rhizobacteria instigated systemically against a broad spectrum of disease- influence the physiology of the plant to a large extent (Alori causing organisms (Millet et al. 2010; Berendsen et al. 2012). et al. 2017), and they can suppress soil borne plant pathogens Plant pathogens pose a prolonged threat to food production through the stimulation of plant-induced systemic resistance at a global scale (Devi et al. 2018). Synthetic agrochemicals and the production of nematicidal, antiviral, and antimicrobial are frequently used in protecting plants from disease-causing substances (Doornbos et al. 2012). Plant growth-promoting organisms. However, unselective application of the synthetic bacteria are able to suppress pathogenic organisms by using agrochemicals can cause numerous adverse effects on human the mechanism (Fig. 3) of producing siderophore, lytic en- and environmental health (Mahdi et al. 2010). Recently, mi- zymes, antibiotics, fluorescent pigments, and cyanides crobial inoculants have been used as an ecologically friendly (Babalola 2010; Olanrewaju et al. 2017) or by consuming approach in suppressing or fighting plant pathogens (Ayitso compounds which stimulate the pathogens and competing et al. 2015). Termite mound material is seen as an ecologically with the pathogens for nutrients (Berg 2009; Doornbos et al. friendly method for reducing inorganic fertilizers through bi- 2012). For instance, Pseudomonas fluorescens WCS417 sup- ological activities, as they are loaded with microorganisms press flagellin triggered by immune responses through capable of suppressing soil borne plant pathogens and Fig. 3 Mechanisms used by plant growth-promoting bacteria to suppress plant pathogenic organisms Ann Microbiol (2019) 69:211–219 217 Publisher’snote Springer Nature remains neutral with regard to jurisdic- mobilizing vital nutritional elements in soil (Bama and tional claims in published maps and institutional affiliations. Ravindran 2012; Devi et al. 2018). Chauhan et al. (2016) reported that B. endophyticus TSH42 and B. cereus TSH77 isolated from termite mound soil significantly slow down the References growth of Fusarium solani (a plant pathogen causing rot dis- ease in crops like potato). Investigation of the acidified cell- Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubi- free culture filtrate using liquid chromatography–mass spec- lization and its potential for use in sustainable agriculture. Front trometry showed that B. cereus TSH77 are made up of Microbiol 8:971 Arumugam M, Pushpanathan M, Sathyavathi S, Gunasekaran P, fengycin and surfactin while B. endophyticus TSH42 Rajendhran J (2016) Comparative analysis of microbial diversity contained fengycin, surfactin, and iturin. The rhizome rot dis- in termite gut and termite nest using ion sequencing. Curr eases in Curcuma longa L. were controlled, when treated with Microbiol 72:267–275 three strains of these bacteria. Staphylococcus saprophyticus Ayitso AS, Onyango DM, Wagai SO (2015) Antimicrobial activities of microorganisms obtained from the gut of Macrotermes michaelseni and Bacillus methylotrophicus isolated from termite mound in Maseno, Kenya. 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BMC Biotechnol 11(1):94 survival benefit to the termites when exposed to M. anisopliae Batalha L, Da Silva Filho D, Martius C (1995) Using termite nests as a (Chouvenc et al. 2013). source of organic matter in agrosilvicultural production systems in Amazonia. Sci Agric 52(2):318–325 Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486 Berg G (2009) Plant–microbe interactions promoting plant growth and Concluding remarks and future directions health: perspectives for controlled use of microorganisms in agricul- ture. Appl Microbiol Biotechnol 84(1):11–18 Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers func- With the quest to produce more agricultural crops for the ever tion as key player in sustainable agriculture by improving soil fer- increasing human population, there is a need to accomplish tility, plant tolerance and crop productivity. Microb Cell Factories that quest without compromising the safety of the environ- 13(1):66 ment or human health. As a result of the grave health and Bignell DE (2010) Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland biology of environmental problems associated with the use of chemical termites: a modern synthesis. Springer, Dordrecht, pp 375–412 fertilizers and pesticides globally, there is a need for alterna- Brune A, Ohkuma M (2010) Role of the termite gut microbiota in sym- tive safe measures. Termite mound soil contains useful bacte- biotic digestion biology of termites: a modern synthesis. Springer, ria that are capable of decomposing lignin and cellulose, fix- Dordrecht, pp 439–475 ing nitrogen, solubilizing phosphate, and suppressing plant Chakdar H, Dastager SG, Khire JM, Rane D, Dharne MS (2018) Characterization of mineral phosphate solubilizing and plant growth soil pathogens. These have put them in a position to function promoting bacteria from termite soil of arid region. Biotech 8(11): as biofertilizers and biocontrol. For the future success of ter- 463. https://doi.org/10.1007/s13205-018-1488-4 mite mound soil usage as biofertilizers and biocontrol, exten- Chauhan AK, Maheshwari DK, Kim K, Bajpai VK (2016) Termitarium- sive research is still required to unveil their full potential. inhabiting Bacillus endophyticus TSH42 and Bacillus cereus TSH77 colonizing Curcuma longa L.: isolation, characterization, and evaluation of their biocontrol and plant-growth-promoting ac- Author contributions B.J.E. wrote the first draft. O.O.B. provided the tivities. Can J Microbiol 62(10):880–892 academic input and thoroughly critiqued the article. Both authors ap- Chauhan AK, Maheshwari DK, Dheeman S, Bajpai VK (2017) proved the article for publication. Termitarium-inhabiting Bacillus spp. enhanced plant growth and bioactive component in turmeric (Curcuma longa L.). Curr Funding Information Support to B.J.E.’s Doctoral program was provid- Microbiol 74(2):184–192 ed by the South Africa’s National Research Foundation/The World Choudhary M, Datta A, Jat HS et al (2018) Changes in soil biology under Academy of Science African Renaissance grant (UID110909). The conservation agriculture based sustainable intensification of cereal National Research Foundation, South Africa for the grant (UID81192) systems in indo-Gangetic Plains. Geoderma 313:193–204 provided support to O.O.B. that has supported research in her lab. Chouvenc T, Efstathion CA, Elliott ML, Su N-Y (2013) Extended disease resistance emerging from the faecal nest of a subterranean termite. Compliance with ethical standards Proc R Soc Biol Sci 280(1770):1–9 Chowdhury SP, Hartmann A, Gao X, Borriss R (2015) Biocontrol mech- anism by root-associated Bacillus amyloliquefaciens FZB42–are- Conflict of interest The authors declare that they have no conflict of view. 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