Abstract

The Fibrobacteres has been recognized as a bacterial phylum for over a decade, but little is known about the group beyond its environmental distribution, and characterization of its sole cultured representative genus, Fibrobacter, after which the phylum was named. Based on these incomplete data, it is thought that cellulose hydrolysis, anaerobic metabolism, and lack of motility are unifying features of the phylum. There are also contradicting views as to whether an uncultured sister lineage, candidate phylum TG3, should be included in the Fibrobacteres. Recently, chitin-degrading cultured representatives of TG3 were isolated from a hypersaline soda lake, and the genome of one species, Chitinivibrio alkaliphilus, sequenced and described in detail. Here, we performed a comparative analysis of Fibrobacter succinogenes, C. alkaliphilus and eight near or substantially complete Fibrobacteres/TG3 genomes of environmental populations recovered from termite gut, anaerobic digester, and sheep rumen metagenomes. We propose that TG3 should be amalgamated with the Fibrobacteres phylum based on robust monophyly of the two lineages and shared character traits. Polymer hydrolysis, using a distinctive set of glycoside hydrolases and binding domains, appears to be a prominent feature of members of the Fibrobacteres. Not all members of this phylum are strictly anaerobic as some termite gut Fibrobacteres have respiratory chains adapted to the microaerophilic conditions found in this habitat. Contrary to expectations, flagella-based motility is predicted to be an ancestral and common trait in this phylum and has only recently been lost in F. succinogenes and its relatives based on phylogenetic distribution of flagellar genes. Our findings extend current understanding of the Fibrobacteres and provide an improved basis for further investigation of this phylum.

Highlights

  • The phylum Fibrobacteres is recognized as a major line of descent in the bacterial domain but is understudied due to limited representation by axenic cultures

  • Bulk DNAs extracted from three lab-scale anaerobic digesters collected at two timepoints [AD1 to 3; reported in Vanwonterghem et al (2014)] were sequenced to produce a total of 111 Gb (2 × 100 bp Illumina reads)

  • We have substantially expanded the phylogenomic representation of the Fibrobacteres and TG3 lineages by obtaining eight draft genomes of environmental populations from termite guts, anaerobic cellulose-fed digester, and a sheep rumen

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Summary

Introduction

The phylum Fibrobacteres is recognized as a major line of descent in the bacterial domain but is understudied due to limited representation by axenic cultures. Fibrobacter currently comprises two species, Fibrobacter succinogenes isolated from a cow rumen (Hungate, 1950) and Fibrobacter intestinalis isolated from a rat cecum (Montgomery and Macy, 1982), of which the former has Phylogenomic Analysis of the Fibrobacteres a publicly available genome sequence (Suen et al, 2011) Both species are primary degraders of cellulosic plant biomass in herbivore guts (Hungate, 1950; Montgomery et al, 1988), which has prompted the suggestion that cellulose degradation may be a unifying feature of the phylum (Ransom-Jones et al, 2012, 2014). There have been conflicting views as to whether TG3 should be merged with the Fibrobacteres or retained as a separate phylum (Sorokin et al, 2014)

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