Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans.

Donato Giovannelli,Costantino Vetriani,Michael Hügler,Thomas Schweder,Stefan M Sievert,Dörte Becher,Stephanie Markert

doi:10.7554/elife.18990

Abstract

Anaerobic thermophiles inhabit relic environments that resemble the early Earth. However, the lineage of these modern organisms co-evolved with our planet. Hence, these organisms carry both ancestral and acquired genes and serve as models to reconstruct early metabolism. Based on comparative genomic and proteomic analyses, we identified two distinct groups of genes in Thermovibrio ammonificans: the first codes for enzymes that do not require oxygen and use substrates of geothermal origin; the second appears to be a more recent acquisition, and may reflect adaptations to cope with the rise of oxygen on Earth. We propose that the ancestor of the Aquificae was originally a hydrogen oxidizing, sulfur reducing bacterium that used a hybrid pathway for CO2 fixation. With the gradual rise of oxygen in the atmosphere, more efficient terminal electron acceptors became available and this lineage acquired genes that increased its metabolic flexibility while retaining ancestral metabolic traits.

Highlights

Deep-branching, anaerobic, thermophilic Bacteria and Archaea inhabit relic environments that resemble the early Earth (Baross and Hoffman, 1985; Martin et al, 2008)
While all four enzymes were detected in the proteomic analysis (Figure 3), we think that the possible involvement of a 5-formyl-THF cycloligase in the synthesis of formyl-THF in T. ammonificans is appealing, as this would provide an evolutionary link between the N5-formate uptake of methanogens and N10formate uptake in acetogens (Braakman and Smith, 2012)
Based on the finding that Group 1 hydrogen oxidation (Hyn) hydrogenases were expressed when T. ammonificans was grown under nitrate-reducing conditions (Figure 3), we suggest that these enzymes are linked through the membrane quinone pool to nitrate reduction and may have been acquired simultaneously with the nap genes

Summary

Introduction

Deep-branching, anaerobic, thermophilic Bacteria and Archaea inhabit relic environments that resemble the early Earth (Baross and Hoffman, 1985; Martin et al, 2008). Their lineages have co-evolved with Earth and their genomes carry more recently acquired traits. These microorganisms can be used as models to reconstruct the evolution of metabolism. Thermovibrio ammonificans is part of the phylum Aquificae, a deep-branching group of thermophilic bacteria found in geothermal environments (Lebedinsky et al, 2007; Sievert and Vetriani, 2012). Based on phylogenetic analyses of the 16S rRNA gene as well as whole genomes, Aquificae

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