H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron
ABSTRACT 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 delete...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-04-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.00076-23 |
| _version_ | 1797839605498642432 |
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| author | Trevor L. Woodard Toshiyuki Ueki Derek R. Lovley |
| author_facet | Trevor L. Woodard Toshiyuki Ueki Derek R. Lovley |
| author_sort | Trevor L. Woodard |
| collection | DOAJ |
| description | ABSTRACT 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. |
| first_indexed | 2024-04-09T16:00:43Z |
| format | Article |
| id | doaj.art-5fb0daec57c549d48737673624e47dae |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-04-09T16:00:43Z |
| publishDate | 2023-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-5fb0daec57c549d48737673624e47dae2023-04-25T13:04:56ZengAmerican Society for MicrobiologymBio2150-75112023-04-0114210.1128/mbio.00076-23H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of IronTrevor L. Woodard0Toshiyuki Ueki1Derek R. Lovley2Department of Microbiology, University of Massachusetts—Amherst, Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts—Amherst, Amherst, Massachusetts, USADepartment of Microbiology, University of Massachusetts—Amherst, Amherst, Massachusetts, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mbio.00076-23Desulfovibrio vulgarisbiocorrosionextracellular electron transferironsulfate reduction |
| spellingShingle | Trevor L. Woodard Toshiyuki Ueki Derek R. Lovley H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron mBio Desulfovibrio vulgaris biocorrosion extracellular electron transfer iron sulfate reduction |
| title | H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron |
| title_full | H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron |
| title_fullStr | H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron |
| title_full_unstemmed | H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron |
| title_short | H2 Is a Major Intermediate in Desulfovibrio vulgaris Corrosion of Iron |
| title_sort | h2 is a major intermediate in desulfovibrio vulgaris corrosion of iron |
| topic | Desulfovibrio vulgaris biocorrosion extracellular electron transfer iron sulfate reduction |
| url | https://journals.asm.org/doi/10.1128/mbio.00076-23 |
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