Metatranscriptomics Reveals the Active Bacterial and Eukaryotic Fibrolytic Communities in the Rumen of Dairy Cow Fed a Mixed Diet.

Sophie Comtet-Marre,Nicolas Parisot,Ali R. Bayat,Pascale Lepercq,Frédérique Chaucheyras-Durand,Eric Peyretaillade,Pierre Peyret,Kevin J. Shingfield,Evelyne Forano,Pascale Mosoni

doi:10.3389/fmicb.2017.00067

Abstract

Ruminants have a unique ability to derive energy from the degradation of plant polysaccharides through the activity of the rumen microbiota. Although this process is well studied in vitro, knowledge gaps remain regarding the relative contribution of the microbiota members and enzymes in vivo. The present study used RNA-sequencing to reveal both the expression of genes encoding carbohydrate-active enzymes (CAZymes) by the rumen microbiota of a lactating dairy cow and the microorganisms forming the fiber-degrading community. Functional analysis identified 12,237 CAZymes, accounting for 1% of the transcripts. The CAZyme profile was dominated by families GH94 (cellobiose-phosphorylase), GH13 (amylase), GH43 and GH10 (hemicellulases), GH9 and GH48 (cellulases), PL11 (pectinase) as well as GH2 and GH3 (oligosaccharidases). Our data support the pivotal role of the most characterized fibrolytic bacteria (Prevotella, Ruminocccus and Fibrobacter), and highlight a substantial, although most probably underestimated, contribution of fungi and ciliate protozoa to polysaccharide degradation. Particularly these results may motivate further exploration of the role and the functions of protozoa in the rumen. Moreover, an important part of the fibrolytic bacterial community remains to be characterized since one third of the CAZyme transcripts originated from distantly related strains. These findings are used to highlight limitations of current metatranscriptomics approaches to understand the functional rumen microbial community and opportunities to circumvent them.

Highlights

The rumen harbors an amazing diversity of microorganisms, comprising prokaryotes and eukaryotes, which cover essential functions for their host
Even though shot-gun metagenomics approaches have been successfully applied in the past to decipher the fibrolytic potential of the rumen microbiota, metatranscriptomics approaches offer the opportunity to investigate the relative contribution of metabolically active members of the rumen microbial community
Using different experimental conditions, the present study completes the available snapshots of the key features of ruminal fiber degradation by confirming the main contributors to this function, and generating new information highlighting the role of eukaryotic microorganisms

Summary

Introduction

The rumen harbors an amazing diversity of microorganisms, comprising prokaryotes (bacteria, archaea) and eukaryotes (protozoa, fungi), which cover essential functions for their host. Part of these microorganisms are specialized in the degradation of plant polysaccharides and thereby constitute a pivotal community providing a supply of energy to the host animal (Hobson and Stewart, 1997; White et al, 2014). Dai et al (2015) and Shinkai et al (2016) conducted a metatranscriptomic survey of the fiber-attached microorganisms in the rumen of cattle confirming the active fibrolytic status of well-known dominant bacterial degraders. The relative contribution of eukaryotes to ruminal fiber degradation was not investigated extensively in these studies

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