Abstract

A nearly complete genome sequence of Candidatus ‘Acetothermum autotrophicum’, a presently uncultivated bacterium in candidate division OP1, was revealed by metagenomic analysis of a subsurface thermophilic microbial mat community. Phylogenetic analysis based on the concatenated sequences of proteins common among 367 prokaryotes suggests that Ca. ‘A. autotrophicum’ is one of the earliest diverging bacterial lineages. It possesses a folate-dependent Wood-Ljungdahl (acetyl-CoA) pathway of CO2 fixation, is predicted to have an acetogenic lifestyle, and possesses the newly discovered archaeal-autotrophic type of bifunctional fructose 1,6-bisphosphate aldolase/phosphatase. A phylogenetic analysis of the core gene cluster of the acethyl-CoA pathway, shared by acetogens, methanogens, some sulfur- and iron-reducers and dechlorinators, supports the hypothesis that the core gene cluster of Ca. ‘A. autotrophicum’ is a particularly ancient bacterial pathway. The habitat, physiology and phylogenetic position of Ca. ‘A. autotrophicum’ support the view that the first bacterial and archaeal lineages were H2-dependent acetogens and methanogenes living in hydrothermal environments.

Highlights

  • Because most deeply branching bacteria are thermophiles, the hypothesis that bacteria arose from a thermophilic ancestor is widely but not universally accepted [1,2]

  • In the pioneering studies of Wachthershauser, the theory of surface metabolism in the early evolution of life was formulated [10], and recently a model for prebiotic cellular and biochemical evolution in an alkaline hydrothermal vent chimney has been proposed with an evolutionary scenario of the acetyl-CoA pathway of CO2 fixation and central intermediary metabolism leading to the synthesis of the constituents of purines and pyrimidines [11,12]

  • Prebiotic cellular and biochemical evolution in an alkaline hydrothermal vent chimney was proposed to involve the acetylCoA pathway of CO2 fixation [10,11]

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Summary

Introduction

Because most deeply branching bacteria are thermophiles, the hypothesis that bacteria arose from a thermophilic ancestor is widely but not universally accepted [1,2]. Since the discovery of deep-sea hydrothermal systems more than 30 years ago, this hypothesis has been supported by the geological and geochemical outlines of early earth environments hosting ancient life [3,4]. In the pioneering studies of Wachthershauser, the theory of surface metabolism in the early evolution of life was formulated [10], and recently a model for prebiotic cellular and biochemical evolution in an alkaline hydrothermal vent chimney has been proposed with an evolutionary scenario of the acetyl-CoA pathway of CO2 fixation and central intermediary metabolism leading to the synthesis of the constituents of purines and pyrimidines [11,12]. A prediction of that view is that the acetyl-CoA pathway should be found in deeply branching bacterial lineages

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