Hydrogenase of the hyperthermophile Pyrococcus furiosus is an elemental sulfur reductase or sulfhydrogenase: evidence for a sulfur-reducing hydrogenase ancestor.

Abstract

Microorganisms growing near and above 100C have recently been discovered near shaflow and deep sea hydrothermal vents. Most are obligately dependent upon the reduction of elemental sulfur (S°) to hydrogen sulfide (H2S) for optimal growth, even though SO reduction readily occurs abioticafly at their growth temperatures. The sulfur reductase activity of the anaerobic archaeon Pyrococcus furiosus, which grows optimally at 100°C by a metabolism that produces H2S if S0 is present, was found in the cytoplasm. It was purified anaerobically and was shown to be identical to the hydrogenase that had been previously purified from this organism. Both S0 and polysulfide served as substrates for H2S production, and the SO reduction activity but not the H2-oxidation activity was enhanced by the redox protein rubredoxin. The H2-oxidizing and SO-reduction activities of the enzyme also showed different responses to pH, temperature, and inhibitors. This bifunctional "sulfhydrogenase" enzyme can, therefore, dispose of the excess reductant generated during fermentation using either protons or polysulfides as the electron acceptor. In addition, purified hydrogenases from both hyperthermophilic and mesophilic representatives of the archaeal and bacterial domains were shown to reduce SO to H2S. It is suggested that the function of some form of ancestral hydrogenase was SO reduction rather than, or in addition to, the reduction of protons.

Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction

“…As archaea participate extensively in the cycling of nitrogen and sulfur (Canfield and Raiswell, 1999;Cabello et al, 2004), and previous 16S rRNA detection of the Thorarchaoeta in anaerobic aquatic sediments is broadly consistent with these geochemical roles, we searched the Thorachaeota genomic bins for the presence of relevant genes. All three of these archaeal bins have homologs to sulfohydrogenase, which has been shown to be involved in the reduction of elemental sulfur in the archaeon P. furiosus (Ma et al, 1993). We found that the Thorarchaeaota bins contain a variety of hydrogenase genes (9-15 per bin).…”

An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia

“…S3). It is unclear whether the M. smegmatis enzyme acts as a bifunctional sulfhydrogenase like its archaeal homologs (39). H 2 S production and media acidification were detected when M. smegmatis became oxygen limited in the presence of 0.1% elemental sulfur.…”

“…Although group 3b [NiFe]-hydrogenases are widespread in actinobacteria and proteobacteria (38), until now, they have only been characterized in thermophilic archaea. Hyd3 shares >30% sequence identity with the cytosolic hydrogenases of Pyrococcus furiosus (39,40) and Thermococcus kodakaraensis (41), including motifs predicted to bind a FAD moiety, a [NiFe] center, and a relay of six [FeS] clusters. Like these enzymes, Hyd3 is likely to evolve H 2 by directly transferring electrons liberated from NAD (P)H at the diaphorase module (hyhG/hyhB) to the [NiFe] center of the hydrogenase module (hyhL/hyhS) (Fig.…”

Evolutionary history of redox metal-binding domains across the tree of life

“…Electrons from H 2 would have been extracted by a membrane-associated hydrogenase and transferred across the membrane to two major pathways: (i) CO 2 reduction in methanogens and (ii) elementary sulfur reduction (38). The latter could have been mediated by a sulfur-reducing hydrogenase ancestor (41) or by an ancient sulfur-reducing domain (42). Interestingly, both of these functions are represented in the largest subnetwork (Fig.…”