Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes

Abstract

In this study, we used shotgun metagenomic sequencing to characterise the microbial metabolic potential for lignocellulose transformation in the gut of two colonies of Argentine higher termite species with different feeding habits, Cortaritermes fulviceps and Nasutitermes aquilinus. Our goal was to assess the microbial community compositions and metabolic capacity, and to identify genes involved in lignocellulose degradation. Individuals from both termite species contained the same five dominant bacterial phyla (Spirochaetes, Firmicutes, Proteobacteria, Fibrobacteres and Bacteroidetes) although with different relative abundances. However, detected functional capacity varied, with C. fulviceps (a grass-wood-feeder) gut microbiome samples containing more genes related to amino acid metabolism, whereas N. aquilinus (a wood-feeder) gut microbiome samples were enriched in genes involved in carbohydrate metabolism and cellulose degradation. The C. fulviceps gut microbiome was enriched specifically in genes coding for debranching-and oligosaccharide-degrading enzymes. These findings suggest an association between the primary food source and the predicted categories of the enzymes present in the gut microbiomes of each species. To further investigate the termite microbiomes as sources of biotechnologically relevant glycosyl hydrolases, a putative GH10 endo-β-1,4xylanase, Xyl10E, was cloned and expressed in Escherichia coli. Functional analysis of the recombinant metagenome-derived enzyme showed high specificity towards beechwood xylan (288.1 IU/mg), with the optimum activity at 50 °C and a pH-activity range from 5 to 10. These characteristics suggest that Xy110E may be a promising candidate for further development in lignocellulose deconstruction applications.

Xylanolytic Extremozymes Retrieved From Environmental Metagenomes: Characteristics, Genetic Engineering, and Applications

“…Further, Zhang et al (2014) studied the role of human gut inhabitant Bacteroidetes by reporting two GH-10 family endoxylanases from the human gut metagenome. Several new findings associated with the xylan-depolymerizing enzymes of metagenomic origin have been published during the past 5 years ( Wang et al, 2015 ; Rashamuse et al, 2016 ; Kim et al, 2018 ; Ellila et al, 2019 ; Alves et al, 2020 ; Victorica et al, 2020 ; Tables 1 , 2 ). Recently, a novel computational method, thermal activity prediction for xylanase (TAXyl), was developed to predict the thermal activity of GH-10 and GH-11 xylanases ( Shahraki et al, 2019 ).…”

“…Whole metagenome sequencing is a relatively more powerful technique over library sequencing to construe the hidden insights of the microbial communities as well as their functional characteristics ( Sharpton, 2014 ; Wiseschart et al, 2019 ). This technique has been adopted to decipher xylan-depolymerizing enzyme-encoding genes from different environmental metagenomes ( Wang et al, 2015 ; Haro-Moreno et al, 2018 ; Lee et al, 2018 ; Victorica et al, 2020 ). Wang et al (2015) reported four β-xylosidases using shotgun sequencing of compost metagenome.…”

Combined whole cell wall analysis and streamlined in silico carbohydrate-active enzyme discovery to improve biocatalytic conversion of agricultural crop residues

“…To provide affordable solutions for optimized lignocellulose degradation, it is common to bioprospect microbial ecosystems of biodigester systems involved in plant biomass saccharification to identify lignocellulose-degrading microorganisms and their endogenous CAZymes. Promising microbes and/or CAZyme targets have been discovered in crop soil [ 155 ], compost [ 156 ], wastewater sludge [ 157 ], and herbivorous animal microbiomes [ 158 , 159 ]. Significantly, the anaerobic environment of the ruminant digestive tract and the termite hindgut has led to the discovery of novel species and microorganisms, including the obligate anaerobic fungi phylum Neocallimastigomycota in cattle rumen [ 160 ] and lignocellulosic microorganisms found in and cultivated by termites [ 159 , 161 ].…”

“…Promising microbes and/ or CAZyme targets have been discovered in crop soil [155], compost [156], wastewater sludge [157], and herbivorous animal microbiomes [158,159]. Significantly, the anaerobic environment of the ruminant digestive tract and the termite hindgut has led to the discovery of novel species and microorganisms, including the obligate anaerobic fungi phylum Neocallimastigomycota in cattle rumen [160] and lignocellulosic microorganisms found in and cultivated by termites [159,161]. Microbial analysis of anaerobic environments is of particular interest to the bioethanol and biogas industries due to the parallels that exist between these environments.…”

Review on Termite Mound Soil Characteristics and Agricultural Importance

“…The dehydrogenase enzyme activity of the fertile soil was found to be > 30 mg TPF/g/h [63]. Most recently a plant cell wall degrading enzyme has been reported in gut micro biomes of Neotropical termite species [64].…”