Isopod holobionts as promising models for lignocellulose degradation

Marius Bredon,Didier Bouchon,Joanne Bertaux,Pierre Grève,Bouziane Moumen,Benjamin Herran

doi:10.1186/s13068-020-01683-2

Abstract

BackgroundIsopods have colonized all environments, partly thanks to their ability to decompose the organic matter. Their enzymatic repertoire, as well as the one of their associated microbiota, has contributed to their colonization success. Together, these holobionts have evolved several interesting life history traits to degrade the plant cell walls, mainly composed of lignocellulose. It has been shown that terrestrial isopods achieve lignocellulose degradation thanks to numerous and diverse CAZymes provided by both the host and its microbiota. Nevertheless, the strategies for lignocellulose degradation seem more diversified in isopods, in particular in aquatic species which are the least studied. Isopods could be an interesting source of valuable enzymes for biotechnological industries of biomass conversion.ResultsTo provide new features on the lignocellulose degradation in isopod holobionts, shotgun sequencing of 36 metagenomes of digestive and non-digestive tissues was performed from several populations of four aquatic and terrestrial isopod species. Combined to the 15 metagenomes of an additional species from our previous study, as well as the host transcriptomes, this large dataset allowed us to identify the CAZymes in both the host and the associated microbial communities. Analyses revealed the dominance of Bacteroidetes and Proteobacteria in the five species, covering 36% and 56% of the total bacterial community, respectively. The identification of CAZymes and new enzymatic systems for lignocellulose degradation, such as PULs, cellulosomes and LPMOs, highlights the richness of the strategies used by the isopods and their associated microbiota.ConclusionsAltogether, our results show that the isopod holobionts are promising models to study lignocellulose degradation. These models can provide new enzymes and relevant lignocellulose-degrading bacteria strains for the biotechnological industries of biomass conversion.

Highlights

Isopods have colonized all environments, partly thanks to their ability to decompose the organic matter
Quality of metagenome and transcriptome assemblies To build the Cazyme repertoire (CAZome) of the isopod holobionts, 51 metagenomic samples from digestive and non-digestive tissues of five isopod species were processed from 36 new datasets, along with 15 datasets from our previous study [25]
Assemblies showed an N50 from 1096 bp to 1523 bp depending on the transcriptome (Additional file 2). They displayed a good completeness since more than 95% of the complete genes from the arthropod core genome were present in the A. vulgare, P. dilatatus dilatatus, P. dilatatus petiti and P. pruinosus assemblies, and 83% of these genes were present in the A. aquaticus assembly (Additional file 2)

Summary

Introduction

Isopods have colonized all environments, partly thanks to their ability to decompose the organic matter Their enzymatic repertoire, as well as the one of their associated microbiota, has contributed to their colonization success. Since the “microbiome revolution” of the last 10 years [2], many studies have highlighted the impact of microbiota on the fitness of the host This change in our vision of organisms led to the recent introduction of the holobiont concept. A holobiont is an assemblage of species that are metabolically interdependent Interaction patterns in these systems shape the holobiont’s composition [6], and bionts (i.e. members of the holobiont) can be agents of developmental plasticity that facilitate the evolution of new phenotypes in animals

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