An Intertwined Evolutionary History of Methanogenic Archaea and Sulfate Reduction

Dwi Susanti,Biswarup Mukhopadhyay,Christos A Ouzounis

doi:10.1371/journal.pone.0045313

Dwi Susanti, Biswarup Mukhopadhyay + Show 1 more

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https://doi.org/10.1371/journal.pone.0045313

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Journal: PloS one	Publication Date: Sep 21, 2012
Citations: 39	License type: CC BY 4.0

Affiliation: Virginia Tech

Abstract

Hydrogenotrophic methanogenesis and dissimilatory sulfate reduction, two of the oldest energy conserving respiratory systems on Earth, apparently could not have evolved in the same host, as sulfite, an intermediate of sulfate reduction, inhibits methanogenesis. However, certain methanogenic archaea metabolize sulfite employing a deazaflavin cofactor (F420)-dependent sulfite reductase (Fsr) where N- and C-terminal halves (Fsr-N and Fsr-C) are homologs of F420H2 dehydrogenase and dissimilatory sulfite reductase (Dsr), respectively. From genome analysis we found that Fsr was likely assembled from freestanding Fsr-N homologs and Dsr-like proteins (Dsr-LP), both being abundant in methanogens. Dsr-LPs fell into two groups defined by following sequence features: Group I (simplest), carrying a coupled siroheme-[Fe4-S4] cluster and sulfite-binding Arg/Lys residues; Group III (most complex), with group I features, a Dsr-type peripheral [Fe4-S4] cluster and an additional [Fe4-S4] cluster. Group II Dsr-LPs with group I features and a Dsr-type peripheral [Fe4-S4] cluster were proposed as evolutionary intermediates. Group III is the precursor of Fsr-C. The freestanding Fsr-N homologs serve as F420H2 dehydrogenase unit of a putative novel glutamate synthase, previously described membrane-bound electron transport system in methanogens and of assimilatory type sulfite reductases in certain haloarchaea. Among archaea, only methanogens carried Dsr-LPs. They also possessed homologs of sulfate activation and reduction enzymes. This suggested a shared evolutionary history for methanogenesis and sulfate reduction, and Dsr-LPs could have been the source of the oldest (3.47-Gyr ago) biologically produced sulfide deposit.

Highlights

Hydrogen-dependent dissimilatory sulfate reduction (4H2+SO422+H+RHS2+4H2O) is one of the oldest energy conserving respiratory systems on Earth that developed about 3.5 billion years ago [1,2,3,4]
It is generally considered that the dissimilatory sulfate reduction system including dsr originated in the bacteria, and the sulfate reducing archaea acquired these through horizontal gene transfer [3,6]
The synthesis presented below is based on the known structurefunction relationships of Fsr, dissimilatory sulfite reductases and assimilatory sulfite reductases (Dsr and aSir) [20,21,22,23]

Summary

Introduction

Hydrogen-dependent dissimilatory sulfate reduction (4H2+SO422+H+RHS2+4H2O) is one of the oldest energy conserving respiratory systems on Earth that developed about 3.5 billion years ago [1,2,3,4]. For Methanocaldococcus jannaschii, a hydrogenotrophic and autotrophic methanogen that lives in the deep-sea hydrothermal vents, this ability is due to a new type of sulfite reductase (Fsr) that utilizes coenzyme F420 as the electron carrier [15,17] (Fig. 1). This possibility is supported by the observation that Methanococcoides burtonii, a methanogen that is phylogenetically closely related to ANME-1 and lives in an environment that is similar to the habitat of ANME-1 [33], carries an Fsr homolog (Fig. 2).

Results

Conclusion