Integrative omics analysis of the termite gut system adaptation to Miscanthus diet identifies lignocellulose degradation enzymes

Abstract

Miscanthus sp. biomass could satisfy future biorefinery value chains. However, its use is largely untapped due to high recalcitrance. The termite and its gut microbiome are considered the most efficient lignocellulose degrading system in nature. Here, we investigate at holobiont level the dynamic adaptation of Cortaritermes sp. to imposed Miscanthus diet, with a long-term objective of overcoming lignocellulose recalcitrance. We use an integrative omics approach combined with enzymatic characterisation of carbohydrate active enzymes from termite gut Fibrobacteres and Spirochaetae. Modified gene expression profiles of gut bacteria suggest a shift towards utilisation of cellulose and arabinoxylan, two main components of Miscanthus lignocellulose. Low identity of reconstructed microbial genomes to closely related species supports the hypothesis of a strong phylogenetic relationship between host and its gut microbiome. This study provides a framework for better understanding the complex lignocellulose degradation by the higher termite gut system and paves a road towards its future bioprospecting.

In their sister’s footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

“…With regards to metabolic potentials of individual symbionts screened in the present study, the distributions of the newly explored functions suggest that these ancient symbionts may occupy unique metabolic niches within the micro-ecosystems of the turtle ant gut compartments, similar to the ancient gut bacterial symbionts of herbivorous honeybees [52], termites [168] and possibly passalid beetles [169]. These results contrast with the previously identified near-ubiquity of amino acid biosynthesis among core turtle ant adult-enriched symbionts [58].…”

Diversity structure of the microbial communities in the guts of four neotropical termite species

“…In accordance with our study, other researchers have reported Spirochaetes as one of the most abundant phyla in wood- and grass-feeding higher termite guts ( Hongoh et al, 2005 ; Warnecke et al, 2007 ; Köhler et al, 2012 ; Brune, 2014 ; Dietrich et al, 2014 ; Mikaelyan et al, 2015 ; Rahman et al, 2015 ). In the last years the majority of glycosyl hydrolase genes encoding putative cellulases and hemicellulases, identified by metagenomic and metatranscriptomic studies, have been associated with Spirochaetes, Fibrobacteres, Bacteroidetes and Firmicutes ( Warnecke et al, 2007 ; He et al, 2013 ; Ben Guerrero et al, 2015 ; Grieco et al, 2019 ; Calusinska et al, 2020 ; Marynowska et al, 2020 ; Romero Victorica et al, 2020 ).…”

“…Nevertheless, for each feeding source, a grouping of bacterial phylotypes by termite subfamily related to the taxonomy of the host was evidenced ( Mikaelyan et al, 2015 ). Furthermore, Calusinska et al (2020) investigated the adaptation of two higher termite colonies ( Cortaritermes sp.) to Miscanthus (a perennial grass) consumption on laboratory conditions and constated the development of a diet-driven, adapted microbial consortium.…”

Evaluation of cellulose degrading bacteria isolated from the gut-system of cotton bollworm, Helicoverpa armigera and their potential values in biomass conversion

“…Thus, majority of the insects including termites and beetles still rely on symbiosis with gut-microorganisms such as bacteria or protozoa, for this repertoire (Xie et al, 2014). Due to this emblematic symbiosis, most of the termites achieve efficient digestion of lignocellulose (60-90%) with significant contribution from gut bacteria (Calusinka et al, 2020). Moreover, the fundamental structure of insect guts having enormous surface-to volume ratio is shaped to shelter a diversity of bacteria ( (Brune & Carsten, 2015).…”