Abstract
Utilization of unexplored lignocellulolytic microbial resources is in demand due to its ability to degrade the waste-plant biomasses like water-hyacinth or noxious weeds for alternative second-generation biofuel production, i.e., biogas. One such “biotechnological treasure-box” is the herbivorous insect gut-system, as its’ symbionts produce key hydrolytic enzymes like lignocellulases, cellulases, xylanases, and pectinases responsible for degradation of their host’s diet plant-biomasses. In this context, this review revealed such lignocellulolytic gut bacterial populations inhabiting the gut-system of only eight orders viz., Blattodea, Lepidoptera, Isoptera, Coleoptera, Orthoptera, Hemiptera, Hymenoptera, and Diptera among 31 insect orders. Proteobacteria is the most predominant group found in every case. Regarding enhanced biogas production, gut bacteria from only three insect orders i.e., Blattodea, Coleoptera, and Diptera were explored so far. Therefore, deployment of such gut bacteria with immense lignocellulolytic potentialities can be harnessed as the sustainable bioresource technology for augmented biogas production utilizing waste-plant biomasses.
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1 Introduction
The development of second-generation fuel for replacing fossil fuel usage extends to a higher magnitude, like upgrading biogas production as renewable energy. Day by day, renewable energy systems are becoming more efficient, functional and cheaper, and sharing the total energy consumption cumulatively (LaBelle 2018). Currently, more than two-thirds of all newly installed global power generating capacities are renewable (Mohammed et al. 2019). The increasingly fast rate of renewable energy as biogas production with 85% of energy requirements is projected to be met by renewables 2050 (Abraham et al. 2020). The scarcity of petroleum and coal is one of the significant threats of the contemporary world as well as their combustion leads to various environmental pollution. Biogas' energy holds promise among these renewable energy sources because it is economical, non-hazardous, and eco-sustainable. Alternative energy production as biogas can reduce greenhouse gas emissions and reduce the usage of fossil fuels (Cheng et al. 2017). The thrust area of biogas from other kinds of renewable energy is its characteristics of using organic waste matters and at the same time produces fertiliser, slurry and clean water for use in agricultural irrigation (Mwirigi et al. 2014). Despite the advantages of the anaerobic digestion (AD) process, the technology has suffered drawbacks in low methane yields, incomplete bioconversion, process instability, and low calorific values. So, to overcome these constraints, a sustainable approach like bioaugmentation with lignocellulolytic bacterial activity appeared as a biotechnological treasure box for human welfare.
Biogas production using AD with different microorganisms such as bacteria, fungi, and archaea with the substrate like cow dung, sewage sludge, etc., is a typical bioaugmentation phenomenon. In the AD process, for the digestion of plant biomass, proficient amount of active inoculum and multifaceted population of microbes catalyse a sequence of inter-reliant biochemical reactions (hydrolysis, acidogenesis, acetogenesis, methanogenesis), is obligatory. Different enzyme-producing microbes, especially bacteria, play a pivotal role in bioaugmented biogas production at each stage of conversion. Like the other conventional processes (physical and chemical pretreatments) for biogas enhancement, biological pretreatment and bioaugmentation get much more attention due to their cleaner and eco-sustainable approaches (Sinha et al. 2021).
Plant biomasses used as substrate in bioenergy production consist of complex compounds, i.e., lignin, cellulose and hemicelluloses. Among these biomass ingredients, lignin is the most complex structure and rigid to degrade. Lignin resists the complete microbial degradation of fermentable organic matters (cellulose and hemicelluloses), and the simpler sugars from the microbial digestion promote bacterial growth and activity by using these sugars as substrates in the fermentation process, leading to the formation of volatile fatty acids and subsequently converted to methane (Sinha et al. 2021). In the bioaugmented plant biomass digestion coordination, the microbial system plays an indispensable role as it recovers the required energy from biomass degradation. Unlike the other microorganisms, different groups of bacteria are more productive in degrading the plant constituents in this system. The bacterial communities with their key hydrolytic enzymatic activities, i.e., lignin peroxidases (LIP), manganese peroxidases (MNP), and laccases (LAC), cellulases (endoglucanases, cellobiohydrolases, and β-glucosidases), and hemicellulases (endo-1,4-β-xylanes, β-xylosidase, α-arabinofuranosidase, and esterases) can accelerate the digestion process to enhance biogas production (Sindhu et al. 2016; de Gonzalo et al. 2016; Sinha et al. 2021).
Delignification of plant biomass using bacteria is biotechnologically significant due to several advantages over fungi because bacteria are an attractive source of commercially operated metabolites having large-scale growth efficiency, product versatility, the limited space requirement for cultivation, conveniences in genetic makeup, and susceptibility towards genetic manipulation (Banerjee et al. 2017). Nowadays, researchers focus more on bacteria and their hydrolytic enzymes in “waste-to-bioenergy” production (Bhatt and Tao 2020). Research has largely been performed on bacteria isolated from soil, litter soil, and vegetable waste, but bacteria from lignocellulosic and cellulosic food consuming insect gut systems are less explored in this arena (Banerjee et al. 2021). Among the diverse sources of bacteria, the role of insect gut bacteria on biogas production is studied very little. Insects are well-diversified, and represent the largest species groups with availability in all ecological niches, with more or less one million species in number (Lysenko 1985) having an arthropod lineage (Moran and Telang 1998). Earlier studies have mainly focused on classical techniques to describe the gut microbial community, information regarding their sustainable biotechnological prospects is lacking (Fox-Dobbs et al. 2010). Most insect species are the host to many kinds of microorganisms, especially bacteria, those are adapted as the gut symbionts (Xie et al. 2019), play an indispensable role in the host's digestion, nutrition, immunogenic responses and life cycle development (Douglas 1992; Tanada and Kaya 1993; Engel et al. 2012; Kudo et al. 2019). During the host metabolic activities, insect gut bacteria produce different hydrolytic enzymes, i.e., lignocellulases, cellulases, hemicellulases, xylanases, pectinases, chitinases, and esterases etc. (Appel 2017). With the help of these enzymatic proficiencies, the microbes can be harnessed for other sustainable purposes, i.e., energy production, bioremediation (Yang et al. 2014; Yang et al. 2015), pest control (Fukui et al. 2015), production of antimicrobial compounds, vitamins, amino acids and lactic acids (Salem et al. 2014; Wang et al. 2015; Liang et al. 2018). Still, there is ample scope of the enzyme-producing insect gut bacteria on bioenergy production as this perspective is rarely explored. This review encompasses the bacterial diversity and potentialities of the lignocellulolytic enzyme-producing insect gut symbionts and their possibilities in bioenergy production via plant biomass utilisation as a “green seedling” as well as “welfare economics”.
2 Review methodology
Here, a total of 695 articles, with the keywords of biogas, anaerobic digestion, insect gut bacteria, and enzyme, were carried out on the Web of Science. By using the VOSviewer software, keywords were analysed. Here the keyword occurrences results were outlined to be 12, and a network map was produced using the most used keywords, and the results are listed in Fig. 1. The cluster and the occurrence frequency of the individual keyword were specified by colour and size, and the line between the circles represents links. By the network mapping of the keywords, it can be found that these articles mainly focus on the following four aspects: (1) biogas production by anaerobic digestion with the help of pretreatment (yellow cluster); (2) methane production using lignocellulosic plant biomass via biological pretreatment (green cluster); (3) biofuel generation via cellulosic plant materials (blue cluster); (4) role of insect gut microbiota in the lignocellulose digestion (red cluster). These keywords covered biogas production with the help of AD, various waste biomass and lignocellulase enzyme-producing insect gut bacteria, etc., which helps in the direction of this review article.
3 Plant biomass as a bio-resource for biogas production
Plant biomasses such as agricultural residues and water hyacinth, and other noxious weeds with immense biogas producing credibility were not appropriately exploited during the AD process due to their lignocellulosic complexity, recalcitrant rigidity and hydrophobic impermeability with various biologically stable linkages (Patinvoh et al. 2017). Lignocellulosic biomass is composed of polymeric substances such as cellulose, hemicellulose (fermentable organic matter), and lignin. Cellulose shapes the principal portion of lignocellulose, surrounded by a hemicellulose matrix and the exterior by the lignin layer (Saini et al. 2015). Cellulose consists of more than 100-140,000 D-glucose units and is condensed by β-1,4-glycosidic bonds or linkages and forms a straight-chain polymer. The occurrence of multiple hydroxyl groups on the glucose forms hydrogen bonds that hold the chain and make it steadier. Cellulose is hydrophilic, but its large polymeric structure render it less soluble in water (Karimi and Taherzadeh 2016). The other polymeric constituent of the lignocellulosic biomass is hemicelluloses, which is a heteropolysaccharide with side chains, i.e., major structural unit pentoses (xylans), followed by arrangements of hexoses like mannose, glucose and galactose and sugar acids (d-glucuronic and d-galacturonic acids) (Somerville et al. 2004). Unlike cellulose, hemicelluloses have an amorphous structural integrity and a random degree of polymerisation, making them more prone to physical, chemical, and biological degradation sensitive. Therefore, the digestibility of the plant biomass more or less depends upon the hemicellulose content of the biomass (Li et al. 2015).
Moreover, the fermentable organic layers (cellulose and hemicelluloses) are protected by the hydrophobic lignin heteropolymer and stand as a physical barricade against biological and oxidative digestion, which is the main constrain for the utilisation of lignocellulosic biomass in the AD practices. The spaces between the cellulose and hemicellulose structures are occupied by this lignin constituent of the plant biomass and consist of phenylpropane units (coniferyl, sinapyl, and coumaryl alcohols) and are generally linked by ether bonds (Woiciechowski 2020) (Fig. 2). Due to its hydrophobic characteristics with impermeability and rigidity, high molecular weight and active recalcitrant compound with various biologically stable types' linkages, lignin rich compounds in the AD process needs potential lignocellulase producing microorganisms with unexplored microbial resources like insect gut system etc. In the AD practices, poor methanogenic activity is often observed when single substrates are used due to little organic matter content, imbalanced nutritional inputs in feedstock, rapid acidification, higher nitrogen and heavy metals contents, and long-chain fatty acid generation (Mata-Alvarez et al. 2014). To overcome this problem, using multiple substrates such as agricultural residues (stubbles), noxious weeds, cattle manure, and other organic wastes can be used for co-digestion with potent lignocellulolytic bacteria (Haider et al. 2015). One of the crucial characteristics for optimum bacterial performances (nutrient requirements) for significant energy production during the AD process is the C/N ratio of the substrates. The ideal proportion is ranged between 10 and 35 (Naik et al. 2014), and in the case of stubbles, noxious weeds, water hyacinth, animal food waste, that ratio varied between 50 and 150 (Divya et al. 2015). Therefore, in future, it will be a vital criterion to select the substrates depending upon their C/N ratio for enhanced bioaugmented biogas production systems.
Plant biomass (non-edible) sources such as energy crops, agricultural and forest residues, stubbles, noxious weeds, animal food waste, municipal organic wastes, etc., are commonly utilised for renewable energy production (Sepehri et al. 2020). According to the Indian Agricultural Research Institute (IARI), India generates approximately 2.2 × 106 tons of rice stubble per year (Abdurrahman et al. 2020). In contrast, Lantana camara, a notorious invasive weed, has occupied over 13.2 million hectares of grasslands in India (Negi et al. 2019). In many countries like in India, non-functional crop residues, i.e., stubbles and the noxious weeds abandoned in the field, are burned openly, causes serious air pollutions with the generation of greenhouse gasses such as CO2 (1.5 × 107 tons), CO (9 × 105 tons), SOX (2.5 × 104 tons), particulate matter (1 × 105 tons) and black carbon (5 × 104 tons), as per reported in the year 2020 (Porichha et al. 2021). To transform this pollution into sustainable energy production, such lignocellulosic biomass resources are considered an utmost substrate for bioenergy production in several perspectives like biogas, biohydrogen, bioethanol, etc. Globally, the lignocellulosic biomass production is approximately 120 × 109 tons per annum, equivalent to 2.2 × 1021 Joule, 300 folds more than the current global energy needs (Guo et al. 2015). Crop residues that remained after agricultural practices like stubbles and the noxious weeds like Lantana camara are reflected as a greater foundation of lignocellulosic biomass, and these do not have additional applications (Pandey et al. 2009; Sinha et al. 2021). The resistance that protects the plant biomass from various microbial utilisation is commonly known as the “biomass recalcitrance”, consists of carbohydrate (50% of cellulose and 20% of hemicelluloses) and non-carbohydrate fractions (mainly 25% of lignin and rest of proteins) (Nanda 2013, 2015) that varies from plant to plant (Table 1).
4 Pretreatment strategies for enhanced biogas production
To achieve greater biogas yields from the lignocellulosic biomass, pretreatment is an obligatory approach during AD practice due to the rigid lignocellulosic complexity of the plant biomass. The factors that lead to the confrontation in the biodigestibility of the lignocellulosic biomasses consist of cellulosic crystallinity and degree of polymerisation, porosity and availability of surface area, lignin mediated fortification and hemicellulosic casing to the cellulose matrix etc. (Mosier et al. 2005). In that scenario, the application of pretreatment techniques can accelerate the removal of lignin and digestion of hemicelluloses, followed by the altered crystalline structure of cellulose (Agbor et al. 2011). Additionally, in the AD process, pretreatment helps in increasing the substrate surface area, which escalates more microbial adherence to the lignocellulosic biomass, promotes the substrate-enzyme interactions, and improves the hydrolytic process (Chandra et al. 2015). In this context, several pretreatments based approaches, i.e., physical (mechanical, comminution and irradiation), chemical (acidic, neutral and alkaline hydrolysis, oxidative treatment, organic solvent facilitated, ionic liquids, and alkaline hydrogen peroxide treatment), physicochemical (steam explosion, extrusion, hydrothermal and ammonia fiber expansion) and biological (microbial, i.e., bacterial and enzymatic) techniques are well recognised globally (Kumar et al. 2019). Among these pretreatment practices, biological pretreatment strategies are receiving more acceptance over the other pretreatments owing to their sustainability, less corrosiveness, safe chemical usage, maximum specificity, minimum energy consumption and by-product formation, accessibilities in genetic makeup and susceptibility towards genetic manipulation (Banerjee and Mandal 2020; Sindhu et al. 2016). Pretreatment in AD practice is crucial for the biotransformation of lignocellulosic biomass into fermentable sugar, preferable for microbial growth, nutrition, and optimised hydrolytic enzyme production (Atelge et al. 2020).
On the other hand, the main constraints in physical treatments are high energy requirements (Veluchamy and Kalamdhad 2017), insignificant productivity of methane due to too much size deduction of lignocellulosic biomass (Kumari and Singh 2018), etc. In chemical treatment practice, the major limitations are excess maintenance costs due to the high concentration of acid that leads to corrosion problems (Chen et al. 2017), therefore escalating the purification expenses. Additionally, in this process, some methane inhibitors are formed as byproducts like furfural and 5-hydroxymethyl furfural (5-HMF) which in turn severely reduce the methane yield. Greater alkaline concentrations usage causes degradation and decomposition of polysaccharides, which induce poor methane yield, sodium discharge from sodium hydroxide treatment influences soil salinization, which has serious negative impacts on the environment (Hernández-Beltrán et al. 2019). Moreover, organosolv pretreatment strategy with a chemical catalyst like acids generates acid-catalyzed deterioration of the monosaccharides into furfural and 5-HMF, which subsequently accelerates condensation reactions among lignin and the reactive aldehydes, successively develop low methane production as in acid pretreatment practice (Chaturvedi et al. 2013). Similarly, the main drawback of the ionic liquid application is its high cost. Physicochemical pretreatments also comprised with several limitations like hemicelluloses are partially removed in steam explosion process, and in the case of ammonia fiber expansion practice, recycling of ammonia is necessary, which is also an additional costlier process (Brodeur et al. 2011; Chaturvedi and Verma 2013; Chen et al. 2017; Zhang et al. 2017; Hernández-Beltrán et al. 2019). Overall, the main challenges regarding physical, chemical and physicochemical practices are the formation of methane inhibitors (Atelge et al. 2020) and toxic chemical by-products that can cause severe environmental pollution (Yang et al. 2015). Furthermore, some advanced strategies in the AD techniques have evolved in response to the degradation of lignocellulosic biomass, such as the rumen derived anaerobic digestion (RUDAD) practice and the rumen simulating technique (RUSITEC), where utilisation of digestion mechanisms by the rumen microbial consortia might be better exploited in the design and operation of anaerobic digesters (Bayané et al. 2011).
5 Biological pretreatment
Plant biomass is symbolised for renewable carbon feedstock, which can substitute a substantial level of petroleum-derived fuels. Production of second-generation biofuel from the plant biomasses is a snowballing concept “plant-waste to fuel” where the substrates used in the form of sugarcane bagasse, rice straw, corn straw, corn stover, aquatic macrophytes (water hyacinth) and noxious weed (L. camara) etc. (Table 2). The key challenge in its exploitation is the mainstream of this carbon is entombed in between the recalcitrant polymers like i.e., lignin, cellulose and hemicellulose of the plant cell wall. The deconstruction of lignin is the crucial and challenging footstep in processing lignocellulosic biomass to renewable energy like biogas, biofuel, etc. To conquer this challenge, microbial appliances, as a “biological pretreatment” strategy, performed some molecular tools on lignin depolymerisation as they have developed several deep-seated pathways (Brown and Chang 2014). Biological pretreatment is an eco-sustainable practice that leads to improvised utilization of lignocellulosic biomass and ameliorates the convenience to the enzyme producing microbes, heightening hydrolysis proficiency for greater biogas production (Sindhu et al. 2016). Such pretreatment is commonly associated with applying microbes like bacterial and fungal species, which produces enzymes, i.e., lignin peroxidases, polyphenol oxidases, manganese dependent peroxidases, and laccases etc. capable for digestion of plant biomass substrates like lignin, hemicelluloses and cellulose (Fig. 3).
Enzyme mediated performances are expeditiously attaining attention because of the short catalytic reaction period, low energy consumption, cost-effective, non-hazardous, and environment-sustainable capabilities (Li et al. 2012; Choi et al. 2015). Enzymes of microbial origin are proficiently employed in various industries for greater superiority as well as with an augmented production rate with low cost management and in a non-hazardous approach (Thapa et al. 2020). In the 21st century, the consequences of industrial usage of microbial enzymes have been intensified remarkably and significantly meet the call of a fast-growing population to manage the fatigue of natural resources. Globally, the evaluated value of the industrially potential enzymes is about USD 5.9 billion in 2020 and is predicted to extend USD 8.7 billion by 2026 (Lugani et al. 2021). Microbial enzymatic breakdown of lignocellulosic biomass is essential in mitigating the wastes and generating biofuel (Shah et al. 2015). Microbial pretreatment has several advantages with higher impacts, such as the recovery of the plant biomass's total energy, greater functional diversity, improves productivity, expansion of the enzymatic saccharification, low energy requirement, advanced adaptability (tolerance to several environmental factors like temperature, pH, etc.), as well as its controls the pH during sugar and substrate utilisation (Kalyani et al. 2013; Shrestha et al. 2017; Sharma et al. 2019).
On the other hand, biological pretreatment is also considered a green technology because it has no-chemical usage and curtails the adverse effects of physical and chemical pretreatments (release of toxic chemical by-products) (Sindhu et al. 2016). Among the microbial pretreatment agents, bacteria-mediated pretreatment strategies are more advanced as they shorten the treatment duration due to their fast growth rate and high metabolic activity, vast availability, thermal and chemical stability, and genetic flexibility compared to the fungal system. Moreover, prolonged retention time is required (10–14 days) for coherent fungal growth. Also, fungi consume a significant fraction of carbohydrates used as a raw material for methanogenesis (Hatakka 1994). Therefore, in this type of bacterial pretreatment practice, up to 15% of electricity can be saved, required for ethanolysis in beech wood under bioorganosolv pretreatment (Palmowski and Müller 2000).
Biological pretreatment with bacterial inoculation can assist in sugar recovery up to 75% than the untreated one where Sphingomonas paucimobilis and Bacillus circulans were employed for pretreatment of office paper (Kurakake et al. 2007). Bioconversion of lignocellulosic biomass into fermentable sugar was also documented by Cellulomonas cartae, C. uda, B. maceran, and Zymomonas mobilis in the case of sugar cane bagasse pretreatment (Singh et al. 2008). Banu et al. (2018) reported that B. jerish used in waste activated sludge pretreatment for biomethane production yields 0.279 g COD/ g COD methane. Microbial agents as consortium [0.01% (w/w) for 15 days] can also amplify the digestibility of lignocellulosic biomass (60.9% of lignin and 43% of hemicelluloses) by reducing 34.6% technical digestion time as well as 96.33% higher methane yield (Zhong et al. 2011). In the case of bacterial pretreatment of corn straw, Pseudomonas aeruginosa, Streptomyces badius, and B. circulans can reduce hemicellulose, cellulose, and lignin content by 44.4%, 34.9%, and 39.2%, as well as increases yields of methane up to 14.85 mL/h (Li et al. 2020a) (Table 2). Methane production from microalgae as a substrate can upsurge by 13% when Pseudobutyrivibrio xylanivorans is used as a pretreatment agent (Vidmar et al. 2017).
Currently, the sources of prospective biomolecules with microbial origin have remarkable demand in relation to biotechnological aspects. In this circumstance, exploration of unmapped microbial resources having promising enzymatic potential will be a key way in modern-day’s industrial biotechnology. Among such unexplored natural resources, herbivorous insect gut symbionts, specifically lignocellulolytic bacteria are the true pathfinders as their host diet system are depends on plant biomasses. As per the phenomenon fact that in accordance with the host’s food materials composition, the gut microbes play a pivotal role in host digestion by enzymatic breakdown, therefore, it can be assumed that these endosymbionts may be the good manufacturer of plant biomass digestive enzymes, particularly lignocellulases, cellulases and hemicellulases (Banerjee et al. 2021). Nonetheless, only a few insects orders among the one million insect species with 31 orders have been reported regarding their lignocellulolytic gut microbiota (see supplementary S1-S3). Therefore, insect gut symbionts are full of prospects with a source of biotechnologically potential bio molecules as these microorganisms have to undergo various selection pressures in their host gut system. So there are plenty of possibilities to explore these “biotechnological warhorses” for biological pretreatment.
Both fungi and bacteria have opted for different biochemical processes for lignin disintegration. In this review, the bacterial approaches towards plant biomass utilisation for renewable energy production will be elucidated with modern advances. The bacterial representatives which are involved in the transformation of plant biomass to biogas generation have been reported from different gut environments, such as animal rumen (mainly cow dung), native Australian marsupials, herbivorous insects (termite, caterpillar, cricket, beetle, chafer, cockroach, locust, and agronomic plant pests), and other obligate herbivorous gut systems (Morrison et al. 2009; Banerjee et al. 2016; Gales et al. 2018; Sinha et al. 2021; Zhang et al. 2021). Several research laboratories have documented the digestion of lignocellulosic plant biomasses by the potential insect gut bacteria. Anukam et al. (2020) reported that Morganella morganii, a ligninolytic symbiont from the gut system of Cryptotermes brevis, a wood-feeding termite, can reduce the lignin component up to 53.27% in the case of rice straw digestion. On the other hand, in wheat straw treatment by the gut symbionts of Potosia cuprea, degradation of plant waste biomass extends up to 20% (Gales et al. 2018). Significant plant biomass (saw dust) digestion was also observed by Acinetobacter junii GAC 16.2, a cellulolytic gut bacteria from Gryllotalpa africana (Banerjee et al. 2020). Moreover, Enterobacter hormaechei, a gut isolate of Hypomeces squamosus can digest lignin ingredients of corn straw as high as 32.05% (Zhang et al. 2021). The most promising and studied plant biomass degrading gut symbionts are reported from termites gut system, which can digest up to 74–99% of the cellulose of lignocellulosic biomass (Breznak and Brune 1994).
6 Plant biomass consuming insect gut system: a bioreactor
Insects are among the most diversified and species-rich groups that have transformed to establish themselves in several ecological niches. The steady diversification of this arthropod lineage stands on the plant biomass consumption as these plant biomasses are ubiquitous in nature and the plant cell walls are the major resources for organic carbons on the earth (Banerjee et al. 2021). Insects are well known for ingesting living or dead plant substances as they can consume up to 20% of a crop plant due to their herbivorous food habit, and their choices are ranged from algae to angiosperms (Khan et al. 2010). Sometimes they consume single or multiple plant species or families. On the other side, it is often different plant parts specific to seed or leaves, developing leaf tissues, reproductive or senescing tissues, cell sap, etc. (Bernays and Chapman 2007). Due to their versatile ecological fitness, their requirements are diverse plant ingredients, i.e., starch, cellulose, hemicellulose, lignocellulose, pectin, xylan, tannins, terpenes, esters, glucosinolates, pyrrolizidine alkaloids, and essential amino acids from phloem sap as in the case of Lepidoptera, Diptera, Coleoptera, Isoptera, Orthoptera, Blattodea, and Hemiptera (Banerjee et al. 2021).
Depending on the food habits, especially the plant biomass, the insect gut system produces various lignocellulosic digestive enzymes. In some cases, insects make lignocellulases encoded by their genome (Watanabe 1998) and shatter the food macromolecules into smaller ones. At the same time, insect gut symbionts secrete the majority of the metabolism-specific digestive enzymes such as lignocellulases for the enzymatic digestion of the consumed plant food materials for complete energy mining purposes. Thus, these symbionts execute a pivotal role in aiding host digestion via enhanced digestive proficiency through enzymatic potentiality (Yun et al. 2014; Jing et al. 2020). In the insect gut system, various microbial associations like bacteria, fungi, protozoa, and archaea are present for their beneficial host activities. Insects harbour a rich and diversified microbial community in their gut system (Wiseman 1995). The organisation of the symbiotic association between insects and gut bacteria is deep-rooted and can be exemplified by the Miocene termite Mastotermes electrodominicus, a 20 million-year-old amber fossil that has been found to comprise protists, spirochetes, and other microorganisms (Wier et al. 2002). The insect gut system acts as a continuous culture system where microbes, capable of degrading dietary compounds, are retained and made to multiply, otherwise, microbes lacking this aptitude are washed out (Hayashi et al. 2007). This type of gut symbiotic diversity is principally determined by the host diet or ingested food materials and the environmental habitat (Yun et al. 2014; Kudo et al. 2019).
In this scenario, several reports were documented regarding the lignocellulolytic potentialities of insect gut bacteria. Among the current research outputs, potent cellulase producers such as Acinetobacter junii, Klebsiella pneumoniae, Bacillus licheniformis, B. pumilus, and B. velezensis from the diverse gut system of G. africana (Orthoptera), Diatraea saccharalis (Lepidoptera), Heterotermes indicola (Blattodea), Eudrilus eugeniae (Haplotaxida), and Cyrtotrachelus buqueti (Coleoptera) with 112.38 ± 0.87 U/ml, 30.13 U/mg, 1156 U/mL, 1.480 IU/mL, and 0.752±0.013 U/ml cellulase production were observed, respectively (Shankar et al. 2021; Banerjee et al. 2020; Barbosa et al. 2020; Li et al. 2020b; Afzal et al. 2019) (Table 3). Moreover, hemicellulase (xylanases) producers like Bacillus sp., Arthrobacter sp., and Pseudomonas azotoformans from the different gut systems, i.e., Cryptotermes brevis (Blattodea), Dendroctonus rhizophagus (Coleoptera) with the production of 0.21 U/ml, 2.6 ± 0.07 U/ml, and 10.6 ± 0.66 U/ml of xylanase, respectively were also observed (Tsegaye et al. 2019; Roblero et al. 2017) (Table 4). In the case of the lignocellulase producers such as B. subtilis, Ochrobactrum oryzae, and Dysgonomonas sp. from the different gut systems of Helicoverpa armigera (Lepidoptera), C. brevis (Blattodea), and Cyrtotrachelus buqueti (Coleoptera) produces 179.30 IU/ml, 158.78 IU/ml, 14.6 IU/ml, and 10±0.2 U/ml of lignin peroxidases, respectively (Dar et al. 2021; Luo et al. 2019; Tsegaye et al. 2019) was also documented. Additionally, a significant amount of lignin peroxidase (585.2 U/l) production was also observed by the gut symbiont Enterobacter hormaechei isolated from Hypomeces squamosus (Coleoptera) (Zhang et al. 2021) (Table 5). Pectinase production by the gut symbionts, i.e., B. circulans, P. fluorescens, and Erwinia sp., also experimentally evidenced up to 150±5, 25±5, and 110±5 mU/ml pectiase, respectively, from the gut of Bombyx mori (Lepidoptera) (Anand et al. 2010). Additionally, up to 1.08 IU/ml pectinase produced by Aeromonas hydrophila, from the Coleopteran gut habitat (Onitis philemon) has been reported (Surabhi et al. 2018) (Table 6).
In addition to the lignocellulolytic enzyme producing proficiency of these symbionts, the insect gut system can also act as a bioreactor where these symbionts perform acetogenesis and methanogenesis. One such example is the gut system of Drosophila melanogaster, where the symbiont Acetobactor pomorum promotes acetic acid production (Crotti et al. 2010). Whereas, in the case of Scarab larval gut system, particularly the hindgut, was characterised by an anaerobic condition with a high concentration of volatile fatty acids (VFA) with fermenting bacteria which especially endorses methanogenesis by utilising the VFA as substrates (Huang 2010). Moreover, Bayon and Etiévant (1980) also reported methanogenic bacteria in the proctodeum of Oryctes sp. Zhang et al. (2021) reported biogas production by Enterobacter hormaechei, a gut symbiont of Hypomeces squamosus can generate 59.19 l/kg-VS biogas with methane yield of 14.76 l/kg-VS utilising corn straw as lignocellulosic plant biomass. Interestingly, a commercial scale based production of up to 950 l/kg VS biogas with 57% methane, using L. camara biomass, was also observed from the gut bacteria Microbacterium sp. of Microtermes obesi (Sinha et al. 2021).
Keeping these points in view, the presence of such immense potential of bacterial population with cellulase, lignocellulase, xylanase, and pectinase production capabilities as well as by the performances like acetogenesis, methanogenesis, and biogas production such diversified insect gut bacterial community can act as a pathfinder for modern-days second-generation renewable energy production as biofuel or biogas by utilising lignocellulosic plant biomass.
7 Diversity and distribution of lignocellulolytic enzyme producing insect gut bacteria
Nowadays, the role of insect gut bacteria in the arena of renewable energy production is receiving attention, but the significant application to translate scientific advances into commercial reality is not getting much recognition. So, there is ample scope to explore these gut bacterial populations as a new horizon for integrating biotechnological tools for biogas or biofuel production (Angelidaki et al. 2018). In these circumstances, augmented biogas production via enzymatic degradation (cellulase, lignocellulase, xylanase, and pectinase) potentiality of plant biomasses, exploitation of the insect gut systems has been scrutinised, and so far they belong to only three insect orders, i.e., Blattodea, Coleoptera, and Diptera, among the thirty one insect order (Kavitha et al. 2014; Xiao et al. 2018; Sinha et al. 2021; Zhang et al. 2021). Whereas, in case of the reported insect orders, those are harbouring the gut bacterial community responsible for plant biomass degrading potentialities, with the quantified amount of cellulase, lignocellulase, xylanase and pectinase production, are listed within six orders (Blattodea, Coleoptera, Diptera, Lepidoptera, Isoptera, and Orthoptera) only, among the 31 insect orders. In this case, the highest number of cellulase and pectinase producers belong to the Coleoptera and Lepidopteran gut systems. The xylanase and lignocellulase producers of the bacterial population mainly represents Coleoptera, Blattodea and Lepidopteran gut environment (Fig. 4a). Moreover, the most governing bacterial phylum is the Firmicutes and Proteobacteria, respectively, from the quantified lignocellulolytic enzyme producing insect gut residents (Fig. 4b).
The overall distribution of the non-quantified plant biomass degrading lignocellulolytic enzyme (cellulase, lignocellulase, xylanase, and pectinase) producing insect gut bacterial population (Firmicutes, Proteobacteria, Actinobacteria, Bacteroidetes, and Spirochaetes) revealed that Blattodea is the supreme reservoir of lignocellulase and cellulase producing bacterial community and among them, Proteobacteria are the predominant one. Whereas, in terms of xylanase and pectinase producing gut bacterial communities, Proteobacteria are the leading inhabitants of the Lepidoptera gut system (Fig. 5). Proteobacteria and Firmicutes members are primarily liable for the lignocellulase and cellulase producing proficiency within the most reported gut environment, i.e., Blattodea, Isoptera, and Coleoptera in both the cases, respectively (Fig. 6a, b). The Actinobacterial community are principally recognised for their lignocellulase, cellulase, and xylanase activity from the residents of mostly Blattodea, Isoptera, and Coleoptera gut (Fig. 6c). Bacteroidetes are acknowledged for their lignocellulase and cellulase activity from Blattodea, Coleoptera, Isoptera, and Orthoptera gut systems (Fig. 6d). Spirochaetes are only the gut symbionts of the Isoptera and Coleoptera groups and are responsible for lignocellulase and cellulase production only (Fig. 6e).
In other perspective, the abundance of cellulose degraders are mainly documented in the Coleoptera group, and the leading bacterial phyla are Proteobacteria and Firmicutes, with 33 and 16 numbers of reports. In the case of lignocellulase producers, the most documented gut system is the Blattodea, where the most bacterial representatives are Proteobacteria and Firmicutes with 60 and 28 experimental evidence. Whereas, the xylanase producers are predominantly observed from the gut system of Coleoptera and Lepidoptera with the highest 12 numbers of Proteobacterial evidence. Among the pectinase producers, the leading bacterial member is from the Proteobacteria with four reported studies and mainly residing in the gut of Lepidopterans (Fig. 6a–e).
Therefore, from this review, it can be justified that, in search of unexplored microbial resources for renewable energy production, more exploration of other herbivorous insect gut systems with potent lignocellulolytic symbionts, other than these eight (Blattodea, Coleoptera, Lepidoptera, Isoptera, Diptera, Orthoptera, Hymenoptera, and Hemiptera) reported insect order would be beneficial for fulfilling the next-generation energy demands as well as to achieve sustainable ecosystem also. Lignocellulolytic gut symbionts like Proteobacteria and Firmicutes exhibited their dominancy in plant biomass digestibility, and those can be tied together for greater biogas production.
8 Omics-based projections in the arena of the biogas generating microbial community
Microbiological culture-dependent methods provide only limited knowledge and information, accounting for less than 0.1% of the bacterial community structure, physiological features, and diversity (Stolze et al. 2015). Microbial methane production via the anaerobic digestion process is directly proportional to the microbial community in the anaerobic digester and is a resultant of the various metabolic pathways exercised by the micro-dwellers (Schnürer 2016). This is, in turn, governed by the thermodynamic laws inside the reactor (Schnürer 2016; Campanaro et al. 2018). Microbial biogas generation by converting waste matter yielding methane has been considered a black box setup, and the role of microbiota behind the process has long been unnoticed (Robles et al. 2018). The relation between methane generation and the microbial community composition of the reactor is an inter-linked process, and this paradigm offers to be exploited for improving the efficiency through microbial selection or formulation (Theuerl et al. 2018; Ziels et al. 2018). The complex community of microbes thrives and replaces the various stages of biogas generation; hence, knowledge of the microbial consortia is of utmost importance in augmenting the process.
Metagenome studies of anaerobic digester samples using next-generation sequencing 16S rRNA gene amplicon sequencing empowered researchers with the knowledge of taxonomy outlining biogas generating microbial populations. Profound understanding of microbial communities under laboratory scale (Sträuber et al. 2016; Zhu et al. 2019) and large-scale digesters and biogas plants were carried out recently (Koo et al. 2019; Ma et al. 2021). Metagenome sourced from various anaerobic digesters has helped develop exceptional knowledge about the micro-inhabitants and their characteristic features in biogas generation (see supplementary file). In this regard, metatranscriptome and metaproteome have been the very recent applications of high-throughput sequencing. The first report of metatranscriptome analysis by Zakrzewski et al. (2012) studied the active microbial community of a fabricated biogas plant using the 16S rRNA tags. Analysis of the meta-transcripts revealed encoded enzymes actively carrying out the various methanogenesis processes. A recent investigation in the metabolism of methanogens inside the anaerobic apparatus using coupled metagenomic and metatranscriptomic approaches unveiled the natural system, and Methanosarcina thermophila was shown to be the predominant methanogen (Zhu et al. 2020). Metaproteomic studies targeting the complete protein composition of the diverse microbial anaerobic systems give the perfect image of the multifaceted relationship of microbes with their environment. A metaproteomic study strikingly revealed that microbial communities inside the reactor vessel were shaped by syntrophism and interaction with bacteriophages (Heyer et al. 2019).
In context to the current review of lignocellulose degraders from insect gut, metagenome studies have revealed remarkable populations of microbial degraders with active enzymes for lignin and lignocellulose compound degradation (Joynson et al. 2017). The gut microbiota of insects has been shown to directly decompose the polymeric lignocellulose via its multiple active enzymes at a wide range of temperatures and pH, which suggests that the knowledge and information about these types of consortia can be of much ecological importance (Scully et al. 2013) (see supplementary file). Bio-prospection using the high-end next-generation sequencing tools can be of immense advantage in mitigating the quest for new microbial consortia or enzymes that might one day help curb the energy crisis caused by fossil fuels.
9 Conclusion
To fulfil the global energy demands, enhanced bioenergy production through the unexplored herbivorous insect gut microbial communities, especially Proteobacteria and Firmicutes, and their lignocellulolytic (cellulase, lignocellulase, xylanase, and pectinase) proficiencies can be a “treasure box” with immense biotechnological prospects. The utilisation of waste-plant biomasses like water hyacinth, noxious weeds, and stubbles as substrates can be a true eco-sustainable approach as they cause environmental hazards in other ways. The application of omics-based techniques upon these bacterial symbionts, from the unexplored “Natural Bioreactor”, mainly insect gut system, could be a budding source for various novel key hydrolytic enzymes that can be harnessed in a “Green Seedlings for Human Welfare”. Additionally, deployment of such reported gut symbionts for augmentation of biogas production is in an infant stage, so there is plenty scope for employment of such untouched insect gut symbionts as a “Biotechnological Game-Changer” in the modern-day alternative renewable energy generating arena.
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Acknowledgements
Binoy Kumar Show and Aishiki Banerjee are thankful to BBSRC, United Kingdom [Grant Ref: BB/S011439/1] for financial support and research fellowship. Sandipan Banerjee is thankful to the Department of Biotechnology, Govt. of India, for granting DBT Twinning Project [No. BT/PR25738/NER/95/1329/2017]. Richik GhoshThakur is thankful to the Department of Science and Technology, Govt. of India for financial support [DST (DST/TMD/MI/OMGI/ 2018/14)].
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BKS: Conceptualization, Data curation, Formal analysis, Investigation, Resources, Visualization Roles/Writing-original draft, Writing e review & editing. SB: Conceptualization, Data curation, Formal analysis, Investigation, Resources, Software, Visualization Roles/Writing–original draft, Writing e review & editing. AB: Formal analysis, Roles/Writing-original draft, Writing e review & editing. RGT: Data curation, Software & Formal analysis. AKH: Validation, Writing e review & editing. NCM: Validation, Writing e review & editing. ABR: Conceptualisation, Methodology, Validation, Project administration, Supervision, Writing e review & editing. SRB: Conceptualisation, Methodology, Validation, Project administration, Supervision, Writing e review & editing. SC: Conceptualisation, Methodology, Validation, Project administration, Supervision, Writing e review & editing.
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Show, B.K., Banerjee, S., Banerjee, A. et al. Insect gut bacteria: a promising tool for enhanced biogas production. Rev Environ Sci Biotechnol 21, 1–25 (2022). https://doi.org/10.1007/s11157-021-09607-8
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DOI: https://doi.org/10.1007/s11157-021-09607-8