Abstract

The structural complexity of lignocellulosic biomass hinders the extraction of cellulose, and it has remained a challenge for decades in the biofuel production process. However, wood-feeding organisms like termite have developed an efficient natural lignocellulolytic system with the help of specialized gut microbial symbionts. Despite having an enormous amount of high-throughput metagenomic data, specific contributions of each individual microbe to achieve this lignocellulolytic functionality remains unclear. The metabolic cross-communication and interdependence that drives the community structure inside the gut microbiota are yet to be explored. We have contrived a species-wide metabolic interaction network of the termite gut-microbiome to have a system-level understanding of metabolic communication. Metagenomic data of Nasutitermes corniger have been analyzed to identify microbial communities in different gut segments. A comprehensive metabolic cross-feeding network of 205 microbes and 265 metabolites was developed using published experimental data. Reconstruction of inter-species influence network elucidated the role of 37 influential microbes to maintain a stable and functional microbiota. Furthermore, in order to understand the natural lignocellulose digestion inside N. corniger gut, the metabolic functionality of each influencer was assessed, which further elucidated 15 crucial hemicellulolytic microbes and their corresponding enzyme machinery.

Highlights

  • Nasutitermes corniger, a wood-feeding higher termite with natural lignocellulose digestion system, can effectively remove 74–99% of cellulose and 65–87% of hemicellulose from woody biomass, leaving the lignin-rich residues as faeces[6]

  • This study focuses on understanding the microbial metabolic cross-communication and the mechanism of lignocellulose digestion in N. corniger gut by constructing a species-wide metabolic interaction network

  • Metabolites that are rarely produced by the microbial populations, like putrescine, methanethiol, 4-aminobutyrate (GABA), trimethylamine, urea, and lithocholic acid were encountered inside the gut microbiota

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Summary

Introduction

Nasutitermes corniger, a wood-feeding higher termite with natural lignocellulose digestion system, can effectively remove 74–99% of cellulose and 65–87% of hemicellulose from woody biomass, leaving the lignin-rich residues as faeces[6]. Each microbial entity is metabolically interacting with diverse community members through the exchange of small metabolites[8]. Communicating microbial symbionts and their enzyme machinery are necessary to accomplish the complex functionality of lignocellulose degradation inside the termite gut. Earlier studies on metagenomics and functional analysis of termite gut microbiota provided crucial insights into predominating microbial genera, for lignocellulose digestion[10,11,12]. This study focuses on understanding the microbial metabolic cross-communication and the mechanism of lignocellulose digestion in N. corniger gut by constructing a species-wide metabolic interaction network. The shotgun metagenomic data was used to identify microbial species in distinct gut compartments of N. corniger. The inter-species influence network demonstrates the substantial effect of various metabolic functionality in a complex microbial niche. To understand the natural bioreactor system inside N. corniger gut, a set of enzyme cocktail has been exemplified with corresponding lignocellulose degraders

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