Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite
Serpentinization, the reaction of water with ultramafic rock, produces reduced, hyperalkaline, and H2-rich fluids that support a variety of hydrogenotrophic microbial metabolisms. Previous work indicates the occurrence of methanogenesis in fluids from the actively serpentinizing Samail Ophiolite in...
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1523912/full |
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| author | Alta E. G. Howells Alta E. G. Howells Lilja M. Quinn Lilja M. Quinn Miguel G. Silva Miguel G. Silva Kylie Akiyama Kylie Akiyama Lucas M. Fifer Lucas M. Fifer Grayson Boyer Srishti Kashyap Kirt Robinson Kirt Robinson Jared Broddrick Everett L. Shock Tori M. Hoehler |
| author_facet | Alta E. G. Howells Alta E. G. Howells Lilja M. Quinn Lilja M. Quinn Miguel G. Silva Miguel G. Silva Kylie Akiyama Kylie Akiyama Lucas M. Fifer Lucas M. Fifer Grayson Boyer Srishti Kashyap Kirt Robinson Kirt Robinson Jared Broddrick Everett L. Shock Tori M. Hoehler |
| author_sort | Alta E. G. Howells |
| collection | DOAJ |
| description | Serpentinization, the reaction of water with ultramafic rock, produces reduced, hyperalkaline, and H2-rich fluids that support a variety of hydrogenotrophic microbial metabolisms. Previous work indicates the occurrence of methanogenesis in fluids from the actively serpentinizing Samail Ophiolite in the Sultanate of Oman. While those fluids contain abundant H2 to fuel hydrogenotrophic methanogenesis (CO2 + 4H2 ➔ CH4 + 2H2O), the concentration of CO2 is very low due to the hyperalkalinity (> pH 11) and geochemistry of the fluids. As a result, species such as formate and acetate may be important as alternative methanogenic substrates. In this study we quantified the impact of inorganic carbon, formate and acetate availability for methanogenic metabolisms, across a range of fluid chemistries, in terms of (1) the potential diffusive flux of substrates to the cell, (2) the Affinity (Gibbs energy change) associated with methanogenic metabolism, and (3) the energy “inventory” per kg fluid. In parallel, we assessed the genomic potential for the conduct of those three methanogenic modes across the same set of fluids and consider the results within the quantitative framework of energy availability. We find that formatotrophic methanogenesis affords a higher Affinity (greater energetic yield) than acetoclastic and hydrogenotrophic methanogenesis in pristine serpentinized fluids and, in agreement with previous studies, find genomic evidence for a methanogen of the genus Methanobacterium to carry out formatotrophic and hydrogenotrophic methanogenesis, with the possibility of even using bicarbonate as a supply of CO2. Acetoclastic methanogenesis is also shown to be energetically favorable in these fluids, and we report the first detection of a potential acetoclastic methanogen of the family Methanosarcinaceae, which forms a distinct clade with a genome from the serpentinizing seafloor hydrothermal vent field, Lost City. These results demonstrate the applicability of an energy availability framework for interpreting methanogen ecology in serpentinizing systems. |
| format | Article |
| id | doaj-art-d6d096fc1ee34e94b15587eaa0de633a |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-d6d096fc1ee34e94b15587eaa0de633a2025-01-31T09:03:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.15239121523912Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail OphioliteAlta E. G. Howells0Alta E. G. Howells1Lilja M. Quinn2Lilja M. Quinn3Miguel G. Silva4Miguel G. Silva5Kylie Akiyama6Kylie Akiyama7Lucas M. Fifer8Lucas M. Fifer9Grayson Boyer10Srishti Kashyap11Kirt Robinson12Kirt Robinson13Jared Broddrick14Everett L. Shock15Tori M. Hoehler16NASA Ames Research Center, Moffett Field, CA, United StatesBlue Marble Space Institute of Sciences, San Francisco, CA, United StatesBlue Marble Space Institute of Sciences, San Francisco, CA, United StatesDepartment of Biology, Washington University, St. Louis, MO, United StatesBlue Marble Space Institute of Sciences, San Francisco, CA, United StatesDepartment of Aeronautics and Astronautics, Stanford University, Palo Alto, CA, United StatesBlue Marble Space Institute of Sciences, San Francisco, CA, United StatesDepartment of Bioengineering, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Earth and Space Sciences, University of Washington, Seattle, WA, United StatesAstrobiology Program, University of Washington, Seattle, WA, United StatesSchool of Earth and Space Exploration, Arizona State University, Tempe, AZ, United StatesDepartment of Geological Sciences, University of Colorado, Boulder, CO, United StatesBlue Marble Space Institute of Sciences, San Francisco, CA, United StatesSchool of Earth and Space Exploration, Arizona State University, Tempe, AZ, United StatesNASA Ames Research Center, Moffett Field, CA, United StatesSchool of Earth and Space Exploration, Arizona State University, Tempe, AZ, United StatesNASA Ames Research Center, Moffett Field, CA, United StatesSerpentinization, the reaction of water with ultramafic rock, produces reduced, hyperalkaline, and H2-rich fluids that support a variety of hydrogenotrophic microbial metabolisms. Previous work indicates the occurrence of methanogenesis in fluids from the actively serpentinizing Samail Ophiolite in the Sultanate of Oman. While those fluids contain abundant H2 to fuel hydrogenotrophic methanogenesis (CO2 + 4H2 ➔ CH4 + 2H2O), the concentration of CO2 is very low due to the hyperalkalinity (> pH 11) and geochemistry of the fluids. As a result, species such as formate and acetate may be important as alternative methanogenic substrates. In this study we quantified the impact of inorganic carbon, formate and acetate availability for methanogenic metabolisms, across a range of fluid chemistries, in terms of (1) the potential diffusive flux of substrates to the cell, (2) the Affinity (Gibbs energy change) associated with methanogenic metabolism, and (3) the energy “inventory” per kg fluid. In parallel, we assessed the genomic potential for the conduct of those three methanogenic modes across the same set of fluids and consider the results within the quantitative framework of energy availability. We find that formatotrophic methanogenesis affords a higher Affinity (greater energetic yield) than acetoclastic and hydrogenotrophic methanogenesis in pristine serpentinized fluids and, in agreement with previous studies, find genomic evidence for a methanogen of the genus Methanobacterium to carry out formatotrophic and hydrogenotrophic methanogenesis, with the possibility of even using bicarbonate as a supply of CO2. Acetoclastic methanogenesis is also shown to be energetically favorable in these fluids, and we report the first detection of a potential acetoclastic methanogen of the family Methanosarcinaceae, which forms a distinct clade with a genome from the serpentinizing seafloor hydrothermal vent field, Lost City. These results demonstrate the applicability of an energy availability framework for interpreting methanogen ecology in serpentinizing systems.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1523912/fullmethanogenesisserpentinizationsubstrate fluxbioenergeticsgenomics |
| spellingShingle | Alta E. G. Howells Alta E. G. Howells Lilja M. Quinn Lilja M. Quinn Miguel G. Silva Miguel G. Silva Kylie Akiyama Kylie Akiyama Lucas M. Fifer Lucas M. Fifer Grayson Boyer Srishti Kashyap Kirt Robinson Kirt Robinson Jared Broddrick Everett L. Shock Tori M. Hoehler Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite Frontiers in Microbiology methanogenesis serpentinization substrate flux bioenergetics genomics |
| title | Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite |
| title_full | Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite |
| title_fullStr | Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite |
| title_full_unstemmed | Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite |
| title_short | Energetic and genomic potential for hydrogenotrophic, formatotrophic, and acetoclastic methanogenesis in surface-expressed serpentinized fluids of the Samail Ophiolite |
| title_sort | energetic and genomic potential for hydrogenotrophic formatotrophic and acetoclastic methanogenesis in surface expressed serpentinized fluids of the samail ophiolite |
| topic | methanogenesis serpentinization substrate flux bioenergetics genomics |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1523912/full |
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