H₂ Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron

Desulfovibrio vulgaris has been a primary pure culture sulfate reducer for developing microbial corrosion concepts. Multiple mechanisms for how it accepts electrons from Fe⁰ have been proposed. We investigated Fe⁰ oxidation with a mutant of D. vulgaris in which hydrogenase genes were deleted. The hydrogenase mutant grew as well as the parental strain with lactate as the electron donor, but unlike the parental strain, it was not able to grow on H₂. The parental strain reduced sulfate with Fe⁰ as the sole electron donor, but the hydrogenase mutant did not. H₂ accumulated over time in Fe⁰ cultures of the hydrogenase mutant and sterile controls but not in parental strain cultures. Sulfide stimulated H₂ production in uninoculated controls apparently by both reacting with Fe⁰ to generate H₂ and facilitating electron transfer from Fe⁰ to H⁺. Parental strain supernatants did not accelerate H₂ production from Fe⁰, ruling out a role for extracellular hydrogenases. Previously proposed electron transfer between Fe⁰ and D. vulgaris via soluble electron shuttles was not evident. The hydrogenase mutant did not reduce sulfate in the presence of Fe⁰ and either riboflavin or anthraquinone-2,6-disulfonate, and these potential electron shuttles did not stimulate parental strain sulfate reduction with Fe⁰ as the electron donor. The results demonstrate that D. vulgaris primarily accepts electrons from Fe⁰ via H₂ as an intermediary electron carrier. These findings clarify the interpretation of previous D. vulgaris corrosion studies and suggest that H₂-mediated electron transfer is an important mechanism for iron corrosion under sulfate-reducing conditions. IMPORTANCE Microbial corrosion of iron in the presence of sulfate-reducing microorganisms is economically significant. There is substantial debate over how microbes accelerate iron corrosion. Tools for genetic manipulation have only been developed for a few Fe(III)-reducing and methanogenic microorganisms known to corrode iron and in each case those microbes were found to accept electrons from Fe⁰ via direct electron transfer. However, iron corrosion is often most intense in the presence of sulfate-reducing microbes. The finding that Desulfovibrio vulgaris relies on H₂ to shuttle electrons between Fe⁰ and cells revives the concept, developed in some of the earliest studies on microbial corrosion, that sulfate reducers consumption of H₂ is a major microbial corrosion mechanism. The results further emphasize that direct Fe⁰-to-microbe electron transfer has yet to be rigorously demonstrated in sulfate-reducing microbes.