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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. B. homolactica is obligately anaerobic and catalyzes 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. This article is protected by copyright. All
rights reserved.