Distribution of a novel DsrEFH sulfur transferase suggests widespread sulfur oxidation capacity in sulfate reducers.

Microbial sulfur cycling is typically divided into an oxidative and a reductive branch, with microbes driving either sulfide oxidation or sulfate reduction distinguished by their genomic setup. Paradoxically, filamentous cable bacteria perform electrogenic sulfide oxidation but contain genes indicative of sulfate reduction, including the reductive type of dissimilatory sulfite reductase (DsrAB), whereas they apparently lack the canonical sulfur transferase DsrEFH essential for sulfur oxidation. AlphaFold2 structure prediction of conserved cable bacteria proteins with unknown functions identified a protein complex resembling canonical DsrEFH (hereafter termed DsrEFH type II). In vitro characterization of heterologously expressed DsrEFH type II confirmed its sulfur transferase function and, together with site-directed mutagenesis, verified that the conserved cysteine, Cys67, is the active sulfur transfer residue. Genes encoding the novel DsrEFH type II were found in 985 prokaryotic genomes. They typically co-occurred with genes for reductive DsrAB in microbes characterized as sulfate reducers or sulfur disproportionators. This study not only fills an important gap in the sulfide oxidation pathway of cable bacteria, but also suggests that a wide range of sulfate reducing bacteria may be more metabolically versatile than currently understood, representing a major shift in the perception of this globally significant physiological group of microorganisms.