Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites

Martyna Marynowska,Rashi Halder,Xavier Goux,Paul Wilmes,Yves Roisin,Philippe Delfosse,Corinne Rouland-Lefèvre,Magdalena Calusinska,Piotr Gawron,David Sillam-Dussès

doi:10.1186/s40168-020-00872-3

Abstract

BackgroundTermites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. They mainly feed on wood and other plant material at different stages of humification. Lignocellulose is often a principal component of such plant diet, and termites largely rely on their symbiotic microbiota and associated enzymes to decompose their food efficiently. While lower termites and their gut flagellates were given larger scientific attention in the past, the gut lignocellulolytic bacteria of higher termites remain less explored. Therefore, in this study, we investigated the structure and function of gut prokaryotic microbiomes from 11 higher termite genera representative of Syntermitinae, Apicotermitinae, Termitidae and Nasutitermitinae subfamilies, broadly grouped into plant fibre- and soil-feeding termite categories.ResultsDespite the different compositional structures of the studied termite gut microbiomes, reflecting well the diet and host lineage, we observed a surprisingly high functional congruency between gut metatranscriptomes from both feeding groups. The abundance of transcripts encoding for carbohydrate active enzymes as well as expression and diversity profiles of assigned glycoside hydrolase families were also similar between plant fibre- and soil-feeding termites. Yet, dietary imprints highlighted subtle metabolic differences specific to each feeding category. Roughly, 0.18% of de novo re-constructed gene transcripts were shared between the different termite gut microbiomes, making each termite gut a unique reservoir of genes encoding for potentially industrially applicable enzymes, e.g. relevant to biomass degradation. Taken together, we demonstrated the functional equivalence in microbial populations across different termite hosts.ConclusionsOur results provide valuable insight into the bacterial component of the termite gut system and significantly expand the inventory of termite prokaryotic genes participating in the deconstruction of plant biomass.7BKR4-UruiiWAwgYk8svodVideo

Highlights

Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services
Compositional structure of bacterial microbiomes in higher termite gut reflects the diet and lineage of the host According to the recent reports, the host diet appears to be the major determinant of the bacterial community structure in higher termite guts [38], and the dietary changes in the feeding routine affect the composition of gut microbiota [39]
To characterise the diversity of microbial communities associated with the termite gut, we analysed 41 gut samples collected from workers of 15 different termite genera with distinctive feeding habits

Summary

Introduction

Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. Termites are eusocial insects that greatly contribute to the carbon and nitrogen cycling in tropical ecosystems and provide multiple other ecosystem services, e.g. litter decomposition, bioturbation or water infiltration [1] They mainly feed on plant material in a form of sound wood or at different stages of humification such as leaf litter, humus, and soil organic matter [2]. Members of the Macrotermitinae subfamily are a unique example of higher termites characterised by an additional exo-symbiosis with Termitomyces fungi that initially predigest the biomass, subsequently consumed by termites Of special interest, it is the prokaryotic component of the termite gut system which contributes to the digestion of plant fibre, and to the host nutrition [6]

Methods

Results

Conclusion