An Intertwined Evolutionary History of Methanogenic Archaea and Sulfate Reduction

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.