An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers
Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H₂. Methanogens and sulfate reducers, and the respective energy processes, are thought to be the dominant players and have been the research foci. Recent investigations showed that, in...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2017
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| Online Access: | http://hdl.handle.net/1721.1/109062 https://orcid.org/0000-0002-1348-9584 |
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| author | Lau, Maggie C. Y. Kieft, Thomas L. Kuloyo, Olukayode Linage-Alvarez, Borja van Heerden, Esta Lindsay, Melody R. Magnabosco, Cara Wang, Wei Wiggins, Jessica B. Guo, Ling Perlman, David H. Kyin, Saw Shwe, Henry H. Harris, Rachel L. Oh, Youmi Yi, Min Joo Purtschert, Roland Slater, Greg F. Wei, Siwen Li, Long Sherwood Lollar, Barbara Onstott, Tullis C. Ono, Shuhei |
| author2 | Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences |
| author_facet | Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Lau, Maggie C. Y. Kieft, Thomas L. Kuloyo, Olukayode Linage-Alvarez, Borja van Heerden, Esta Lindsay, Melody R. Magnabosco, Cara Wang, Wei Wiggins, Jessica B. Guo, Ling Perlman, David H. Kyin, Saw Shwe, Henry H. Harris, Rachel L. Oh, Youmi Yi, Min Joo Purtschert, Roland Slater, Greg F. Wei, Siwen Li, Long Sherwood Lollar, Barbara Onstott, Tullis C. Ono, Shuhei |
| author_sort | Lau, Maggie C. Y. |
| collection | MIT |
| description | Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H₂. Methanogens and sulfate reducers, and the respective energy processes, are thought to be the dominant players and have been the research foci. Recent investigations showed that, in some deep, fluid-filled fractures in the Witwatersrand Basin, South Africa, methanogens contribute <5% of the total DNA and appear to produce sufficient CH₄ to support the rest of the diverse community. This paradoxical situation reflects our lack of knowledge about the in situ metabolic diversity and the overall ecological trophic structure of SLiMEs. Here, we show the active metabolic processes and interactions in one of these communities by combining metatranscriptomic assemblies, metaproteomic and stable isotopic data, and thermodynamic modeling. Dominating the active community are four autotrophic β-proteobacterial genera that are capable of oxidizing sulfur by denitrification, a process that was previously unnoticed in the deep subsurface. They co-occur with sulfate reducers, anaerobic methane oxidizers, and methanogens, which each comprise <5% of the total community. Syntrophic interactions between these microbial groups remove thermodynamic bottlenecks and enable diverse metabolic reactions to occur under the oligotrophic conditions that dominate in the subsurface. The dominance of sulfur oxidizers is explained by the availability of electron donors and acceptors to these microorganisms and the ability of sulfur-oxidizing denitrifiers to gain energy through concomitant S and H₂ oxidation. We demonstrate that SLiMEs support taxonomically and metabolically diverse microorganisms, which, through developing syntrophic partnerships, overcome thermodynamic barriers imposed by the environmental conditions in the deep subsurface. |
| first_indexed | 2024-09-23T11:13:08Z |
| format | Article |
| id | mit-1721.1/109062 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T11:13:08Z |
| publishDate | 2017 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/1090622022-09-27T17:58:29Z An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers Lau, Maggie C. Y. Kieft, Thomas L. Kuloyo, Olukayode Linage-Alvarez, Borja van Heerden, Esta Lindsay, Melody R. Magnabosco, Cara Wang, Wei Wiggins, Jessica B. Guo, Ling Perlman, David H. Kyin, Saw Shwe, Henry H. Harris, Rachel L. Oh, Youmi Yi, Min Joo Purtschert, Roland Slater, Greg F. Wei, Siwen Li, Long Sherwood Lollar, Barbara Onstott, Tullis C. Ono, Shuhei Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Ono, Shuhei Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H₂. Methanogens and sulfate reducers, and the respective energy processes, are thought to be the dominant players and have been the research foci. Recent investigations showed that, in some deep, fluid-filled fractures in the Witwatersrand Basin, South Africa, methanogens contribute <5% of the total DNA and appear to produce sufficient CH₄ to support the rest of the diverse community. This paradoxical situation reflects our lack of knowledge about the in situ metabolic diversity and the overall ecological trophic structure of SLiMEs. Here, we show the active metabolic processes and interactions in one of these communities by combining metatranscriptomic assemblies, metaproteomic and stable isotopic data, and thermodynamic modeling. Dominating the active community are four autotrophic β-proteobacterial genera that are capable of oxidizing sulfur by denitrification, a process that was previously unnoticed in the deep subsurface. They co-occur with sulfate reducers, anaerobic methane oxidizers, and methanogens, which each comprise <5% of the total community. Syntrophic interactions between these microbial groups remove thermodynamic bottlenecks and enable diverse metabolic reactions to occur under the oligotrophic conditions that dominate in the subsurface. The dominance of sulfur oxidizers is explained by the availability of electron donors and acceptors to these microorganisms and the ability of sulfur-oxidizing denitrifiers to gain energy through concomitant S and H₂ oxidation. We demonstrate that SLiMEs support taxonomically and metabolically diverse microorganisms, which, through developing syntrophic partnerships, overcome thermodynamic barriers imposed by the environmental conditions in the deep subsurface. 2017-05-12T19:44:09Z 2017-05-12T19:44:09Z 2016-11 2016-08 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/109062 Lau, Maggie C. Y.; Kieft, Thomas L.; Kuloyo, Olukayode; Linage-Alvarez, Borja; van Heerden, Esta; Lindsay, Melody R.; Magnabosco, Cara, et al. “An Oligotrophic Deep-Subsurface Community Dependent on Syntrophy Is Dominated by Sulfur-Driven Autotrophic Denitrifiers.” Proceedings of the National Academy of Sciences 113, no. 49 (November 2016): E7927–E7936. © 2016 National Academy of Sciences https://orcid.org/0000-0002-1348-9584 en_US http://dx.doi.org/10.1073/pnas.1612244113 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Lau, Maggie C. Y. Kieft, Thomas L. Kuloyo, Olukayode Linage-Alvarez, Borja van Heerden, Esta Lindsay, Melody R. Magnabosco, Cara Wang, Wei Wiggins, Jessica B. Guo, Ling Perlman, David H. Kyin, Saw Shwe, Henry H. Harris, Rachel L. Oh, Youmi Yi, Min Joo Purtschert, Roland Slater, Greg F. Wei, Siwen Li, Long Sherwood Lollar, Barbara Onstott, Tullis C. Ono, Shuhei An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| title | An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| title_full | An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| title_fullStr | An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| title_full_unstemmed | An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| title_short | An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| title_sort | oligotrophic deep subsurface community dependent on syntrophy is dominated by sulfur driven autotrophic denitrifiers |
| url | http://hdl.handle.net/1721.1/109062 https://orcid.org/0000-0002-1348-9584 |
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