Abstract

Spirochetes of the genus Treponema are surprisingly abundant in termite guts, where they play an important role in reductive acetogenesis. Although they occur in all termites investigated, their evolutionary origin is obscure. Here, we isolated the first representative of 'termite gut treponemes' from cockroaches, the closest relatives of termites. Phylogenomic analysis revealed that Breznakiella homolactica gen. nov. sp. nov. represents the most basal lineage of the highly diverse 'termite cluster I', a deep-branching sister group of Treponemataceae (fam. 'Termitinemataceae') that was present already in the cockroach ancestor of termites and subsequently coevolved with its host. Breznakiella homolactica is obligately anaerobic and catalyses the homolactic fermentation of both hexoses and pentoses. Resting cells produced acetate in the presence of oxygen. Genome analysis revealed the presence of pyruvate oxidase and catalase, and a cryptic potential for the formation of acetate, ethanol, formate, CO2 and H2 - the fermentation products of termite gut isolates. Genes encoding key enzymes of reductive acetogenesis, however, are absent, confirming the hypothesis that the ancestral metabolism of the cluster was fermentative, and that the capacity for acetogenesis from H2 plus CO2 - the most intriguing property among termite gut treponemes - was acquired by lateral gene transfer.

Highlights

  • Spirochetes are morphologically distinct bacteria with highly motile, helical cells composed of a protoplasmic cylinder and periplasmic flagella that are enclosed in an outer sheath (Paster, 2015)

  • A notable exception is the hindgut of termites, where spirochetes predominate the bacterial microbiota, in the wood-feeding taxa (Brune, 2014; Mikaelyan et al, 2015a)

  • With the advent of 16S rRNA-gene-based phylogenies, it became clear that almost all termite gut spirochetes fall into the radiation of the genus Treponema, where they form two distinct clades (Berchtold et al, 1994; Ohkuma and Kudo, 1996; Paster et al, 1996)

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Summary

Introduction

Spirochetes (phylum Spirochaetes) are morphologically distinct bacteria with highly motile, helical cells composed of a protoplasmic cylinder and periplasmic flagella that are enclosed in an outer sheath (Paster, 2015). They are widespread in a variety of environments but typically occur only in low numbers. A notable exception is the hindgut of termites, where spirochetes predominate the bacterial microbiota, in the wood-feeding taxa (Brune, 2014; Mikaelyan et al, 2015a) They occur either free-living or associated with cellulolytic protists and can make up more than one-half of the bacterial population (Breznak, 2002; Breznak and Leadbetter, 2006; Ohkuma and Brune, 2011). The other clade, which has been referred to as ‘termite Treponema cluster II’ (Ohkuma et al, 1999; Noda et al, 2003), hereafter ‘termite cluster

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