Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments
IntroductionMolecular hydrogen is produced by the fermentation of organic matter and consumed by organisms including hydrogenotrophic methanogens and sulfate reducers in anoxic marine sediment. The thermodynamic feasibility of these metabolisms depends strongly on organic matter reactivity and hydro...
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Frontiers Media S.A.
2024-11-01
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| author | Gage R. Coon Leketha C. Williams Adrianna Matthews Roberto Diaz Richard T. Kevorkian Douglas E. LaRowe Andrew D. Steen Andrew D. Steen Andrew D. Steen Andrew D. Steen Laura L. Lapham Karen G. Lloyd Karen G. Lloyd |
| author_facet | Gage R. Coon Leketha C. Williams Adrianna Matthews Roberto Diaz Richard T. Kevorkian Douglas E. LaRowe Andrew D. Steen Andrew D. Steen Andrew D. Steen Andrew D. Steen Laura L. Lapham Karen G. Lloyd Karen G. Lloyd |
| author_sort | Gage R. Coon |
| collection | DOAJ |
| description | IntroductionMolecular hydrogen is produced by the fermentation of organic matter and consumed by organisms including hydrogenotrophic methanogens and sulfate reducers in anoxic marine sediment. The thermodynamic feasibility of these metabolisms depends strongly on organic matter reactivity and hydrogen concentrations; low organic matter reactivity and high hydrogen concentrations can inhibit fermentation so when organic matter is poor, fermenters might form syntrophies with methanogens and/or sulfate reducers who alleviate thermodynamic stress by keeping hydrogen concentrations low and tightly controlled. However, it is unclear how these metabolisms effect porewater hydrogen concentrations in natural marine sediments of different organic matter reactivities.MethodsWe measured aqueous concentrations of hydrogen, sulfate, methane, dissolved inorganic carbon, and sulfide with high-depth-resolution and 16S rRNA gene assays in sediment cores with low carbon reactivity in White Oak River (WOR) estuary, North Carolina, and those with high carbon reactivity in Cape Lookout Bight (CLB), North Carolina. We calculated the Gibbs energies of sulfate reduction and hydrogenotrophic methanogenesis.ResultsHydrogen concentrations were significantly higher in the sulfate reduction zone at CLB than WOR (mean: 0.716 vs. 0.437 nM H2) with highly contrasting hydrogen profiles. At WOR, hydrogen was extremely low and invariant (range: 0.41–0.52 nM H2) in the upper 15 cm. Deeper than 15 cm, hydrogen became more variable (range: 0.312–2.56 nM H2) and increased until methane production began at ~30 cm. At CLB, hydrogen was highly variable in the upper 15 cm (range: 0.08–2.18 nM H2). Ratios of inorganic carbon production to sulfate consumption show AOM drives sulfate reduction in WOR while degradation of organics drive sulfate reduction in CLB.DiscussionWe conclude more reactive organic matter increases hydrogen concentrations and their variability in anoxic marine sediments. In our AOM-dominated site, WOR, sulfate reducers have tight control on hydrogen via consortia with fermenters which leads to the lower observed variance due to interspecies hydrogen transfer. After sulfate depletion, hydrogen accumulates and becomes variable, supporting methanogenesis. This suggests that CLB’s more reactive organic matter allows fermentation to occur without tight metabolic coupling of fermenters to sulfate reducers, resulting in high and variable porewater hydrogen concentrations that prevent AOM from occurring through reverse hydrogenotrophic methanogenesis. |
| format | Article |
| id | doaj-art-def9fe602af7439f85fca40c645c8846 |
| institution | OA Journals |
| issn | 1664-302X |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Frontiers Media S.A. |
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| spelling | doaj-art-def9fe602af7439f85fca40c645c88462025-08-20T02:14:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-11-011510.3389/fmicb.2024.14558571455857Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sedimentsGage R. Coon0Leketha C. Williams1Adrianna Matthews2Roberto Diaz3Richard T. Kevorkian4Douglas E. LaRowe5Andrew D. Steen6Andrew D. Steen7Andrew D. Steen8Andrew D. Steen9Laura L. Lapham10Karen G. Lloyd11Karen G. Lloyd12Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Earth Sciences, University of Southern California, Los Angeles, CA, United StatesDepartment of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Earth Sciences, University of Southern California, Los Angeles, CA, United StatesDepartment of Earth and Planetary Sciences, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment Marine and Environmental Biology, University of Southern California, Los Angeles, CA, United StatesChesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, MD, United StatesDepartment of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Earth Sciences, University of Southern California, Los Angeles, CA, United StatesIntroductionMolecular hydrogen is produced by the fermentation of organic matter and consumed by organisms including hydrogenotrophic methanogens and sulfate reducers in anoxic marine sediment. The thermodynamic feasibility of these metabolisms depends strongly on organic matter reactivity and hydrogen concentrations; low organic matter reactivity and high hydrogen concentrations can inhibit fermentation so when organic matter is poor, fermenters might form syntrophies with methanogens and/or sulfate reducers who alleviate thermodynamic stress by keeping hydrogen concentrations low and tightly controlled. However, it is unclear how these metabolisms effect porewater hydrogen concentrations in natural marine sediments of different organic matter reactivities.MethodsWe measured aqueous concentrations of hydrogen, sulfate, methane, dissolved inorganic carbon, and sulfide with high-depth-resolution and 16S rRNA gene assays in sediment cores with low carbon reactivity in White Oak River (WOR) estuary, North Carolina, and those with high carbon reactivity in Cape Lookout Bight (CLB), North Carolina. We calculated the Gibbs energies of sulfate reduction and hydrogenotrophic methanogenesis.ResultsHydrogen concentrations were significantly higher in the sulfate reduction zone at CLB than WOR (mean: 0.716 vs. 0.437 nM H2) with highly contrasting hydrogen profiles. At WOR, hydrogen was extremely low and invariant (range: 0.41–0.52 nM H2) in the upper 15 cm. Deeper than 15 cm, hydrogen became more variable (range: 0.312–2.56 nM H2) and increased until methane production began at ~30 cm. At CLB, hydrogen was highly variable in the upper 15 cm (range: 0.08–2.18 nM H2). Ratios of inorganic carbon production to sulfate consumption show AOM drives sulfate reduction in WOR while degradation of organics drive sulfate reduction in CLB.DiscussionWe conclude more reactive organic matter increases hydrogen concentrations and their variability in anoxic marine sediments. In our AOM-dominated site, WOR, sulfate reducers have tight control on hydrogen via consortia with fermenters which leads to the lower observed variance due to interspecies hydrogen transfer. After sulfate depletion, hydrogen accumulates and becomes variable, supporting methanogenesis. This suggests that CLB’s more reactive organic matter allows fermentation to occur without tight metabolic coupling of fermenters to sulfate reducers, resulting in high and variable porewater hydrogen concentrations that prevent AOM from occurring through reverse hydrogenotrophic methanogenesis.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1455857/fullhydrogenmethaneAOMmethanogenesissulfate reductionthermodynamics |
| spellingShingle | Gage R. Coon Leketha C. Williams Adrianna Matthews Roberto Diaz Richard T. Kevorkian Douglas E. LaRowe Andrew D. Steen Andrew D. Steen Andrew D. Steen Andrew D. Steen Laura L. Lapham Karen G. Lloyd Karen G. Lloyd Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments Frontiers in Microbiology hydrogen methane AOM methanogenesis sulfate reduction thermodynamics |
| title | Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments |
| title_full | Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments |
| title_fullStr | Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments |
| title_full_unstemmed | Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments |
| title_short | Control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments |
| title_sort | control of hydrogen concentrations by microbial sulfate reduction in two contrasting anoxic coastal sediments |
| topic | hydrogen methane AOM methanogenesis sulfate reduction thermodynamics |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1455857/full |
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