Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch-degrader Ruminococcus bromii.

Indrani Mukhopadhya,Paul O Sheridan,Alan W Walker,Edward A Bayer,Jenny Laverde‐Gomez,Sarah Moraïs,William Kelly,Harry J Flint,Philip J Cooper,Athol V Klieve,Nathalie Juge,Darrell Cockburn,Petra Louis,Emmanuelle Crost,Nicole Koropatkin,Ryan Kibler,Sylvia H Duncan,Carlos Sandoval,Diane Ouwerkerk

doi:10.1111/1462-2920.14000

Abstract

Summary Ruminococcus bromii is a dominant member of the human colonic microbiota that plays a ‘keystone’ role in degrading dietary resistant starch. Recent evidence from one strain has uncovered a unique cell surface ‘amylosome’ complex that organizes starch‐degrading enzymes. New genome analysis presented here reveals further features of this complex and shows remarkable conservation of amylosome components between human colonic strains from three different continents and a R. bromii strain from the rumen of Australian cattle. These R. bromii strains encode a narrow spectrum of carbohydrate active enzymes (CAZymes) that reflect extreme specialization in starch utilization. Starch hydrolysis products are taken up mainly as oligosaccharides, with only one strain able to grow on glucose. The human strains, but not the rumen strain, also possess transporters that allow growth on galactose and fructose. R. bromii strains possess a full complement of sporulation and spore germination genes and we demonstrate the ability to form spores that survive exposure to air. Spore formation is likely to be a critical factor in the ecology of this nutritionally highly specialized bacterium, which was previously regarded as ‘non‐sporing’, helping to explain its widespread occurrence in the gut microbiota through the ability to transmit between hosts.

Highlights

Ruminococcaceae are an important family of Firmicutes bacteria within gut microbial communities (La Reau et al, 2016)
Summary Ruminococcus bromii is a dominant member of the human colonic microbiota that plays a ‘keystone’ role in degrading dietary resistant starch
R. bromii strains possess a full complement of sporulation and spore germination genes and we demonstrate the ability to form spores that survive exposure to air

Summary

Introduction

Ruminococcaceae are an important family of Firmicutes bacteria within gut microbial communities (La Reau et al, 2016). These bacteria account for around 20% of the healthy human colonic microbiota based on molecular surveys (Suau et al, 2001) with two species, Faecalibacterium prausnitzii and Ruminococcus bromii, among the four most abundant contributors to the human faecal metagenome in European adults (Zhernakova et al, 2016). Resistant starch (RS), i.e. dietary starch that escapes digestion by host amylases, often provides the largest single source of energy for microbial growth in the human colon and its fermentation is considered to provide health benefits (Nugent, 2005). The primary role played by R. bromii in releasing energy from RS to other members of the microbial community, and the drop in RS fermentation when this species is absent from the community, justifies designating it as a ‘keystone’ species within the human colonic microbiota (Ze et al, 2012; Ze et al, 2013)

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Discussion

Conclusion