Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites.

Vincent Hervé,David Sillam-Dussès,Jan Šobotník,Carsten Dietrich,Pengfei Liu,Andreas Brune,Petr Stiblik

doi:10.7717/peerj.8614

Abstract

“Higher” termites have been able to colonize all tropical and subtropical regions because of their ability to digest lignocellulose with the aid of their prokaryotic gut microbiota. Over the last decade, numerous studies based on 16S rRNA gene amplicon libraries have largely described both the taxonomy and structure of the prokaryotic communities associated with termite guts. Host diet and microenvironmental conditions have emerged as the main factors structuring the microbial assemblages in the different gut compartments. Additionally, these molecular inventories have revealed the existence of termite-specific clusters that indicate coevolutionary processes in numerous prokaryotic lineages. However, for lack of representative isolates, the functional role of most lineages remains unclear. We reconstructed 589 metagenome-assembled genomes (MAGs) from the different gut compartments of eight higher termite species that encompass 17 prokaryotic phyla. By iteratively building genome trees for each clade, we significantly improved the initial automated assignment, frequently up to the genus level. We recovered MAGs from most of the termite-specific clusters in the radiation of, for example, Planctomycetes, Fibrobacteres, Bacteroidetes, Euryarchaeota, Bathyarchaeota, Spirochaetes, Saccharibacteria, and Firmicutes, which to date contained only few or no representative genomes. Moreover, the MAGs included abundant members of the termite gut microbiota. This dataset represents the largest genomic resource for arthropod-associated microorganisms available to date and contributes substantially to populating the tree of life. More importantly, it provides a backbone for studying the metabolic potential of the termite gut microbiota, including the key members involved in carbon and nitrogen biogeochemical cycles, and important clues that may help cultivating representatives of these understudied clades.

Highlights

Termites (Blattodea: Termitoidae) are eusocial insects that have predominantly and successfully colonized tropical and subtropical areas across the world
Metagenomes and metagenome-assembled genomes (MAGs) overview Metagenomic reads were generated from the P1, P3, and P4 proctodeal compartments of the gut of the two termite species E. neotenicus and L. labralis
The present study focused on these 589 MAGs, which showed on average a 38.6-fold coverage (Table S2)

Summary

Introduction

Termites (Blattodea: Termitoidae) are eusocial insects that have predominantly and successfully colonized tropical and subtropical areas across the world. One of the keys to this success is their rare ability to degrade lignocellulose, a very abundant but recalcitrant complex carbon substrate (Cragg et al, 2015). Lignocellulose digestion by termites is attributed to the presence of a specific microbiota colonizing the different gut compartments of the host (Brune, 2014). Higher termites represent the most diverse and taxon-rich clade and form about 85% of the termite generic diversity (Krishna et al, 2013). Their gut morphology is more complex than that of the basal clades, and is characterized by the presence of a mixed-segment and an enlarged proctodeal segment P1. The gut displays strong variations in pH and oxygen partial pressure along the anterior–posterior axis, which creates microenvironments within the gut (Brune, 2014)

Methods

Results

Conclusion