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...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 49; pp. E7927 - E7936 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
06.12.2016
|
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.1612244113 |
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| Abstract | 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. |
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| AbstractList | Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H
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 CH
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 H
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. Microorganisms are known to live in the deep subsurface, kilometers below the photic zone, but the community-wide metabolic networks and trophic structures (the organization of their energy and nutritional hierarchy) remain poorly understood. We show that an active subsurface lithoautotrophic microbial ecosystem (SLiME) under oligotrophic condition exists. Taxonomically and metabolically diverse microorganisms are supported, with sulfur-driven autotrophic denitrifiers predominating in the community. Denitrification is a highly active process in the deep subsurface that evaded recognition in the past. This study highlights the critical role of metabolic cooperation, via syntrophy between subsurface microbial groups, for the survival of the whole community under the oligotrophic conditions that dominate in the subsurface. Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H 2 . 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 CH 4 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 H 2 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. Microorganisms are known to live in the deep subsurface, kilometers below the photic zone, but the community-wide metabolic networks and trophic structures (the organization of their energy and nutritional hierarchy) remain poorly understood. We show that an active subsurface lithoautotrophic microbial ecosystem (SLiME) under oligotrophic condition exists. Taxonomically and metabolically diverse microorganisms are supported, with sulfur-driven autotrophic denitrifiers predominating in the community. Denitrification is a highly active process in the deep subsurface that evaded recognition in the past. This study highlights the critical role of metabolic cooperation, via syntrophy between subsurface microbial groups, for the survival of the whole community under the oligotrophic conditions that dominate in the subsurface. Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H 2 . 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 CH 4 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 H 2 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. 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.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. Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H^sub 2^. 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 CH^sub 4^ 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 ...-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 H^sub 2^ 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. (ProQuest: ... denotes formulae/symbols omitted.) 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. |
| Author | Perlman, David H. Wang, Wei Lindsay, Melody R. Purtschert, Roland Li, Long Lollar, Barbara Sherwood Ono, Shuhei Kieft, Thomas L. Yi, Min Joo Oh, Youmi Linage-Alvarez, Borja Magnabosco, Cara Wiggins, Jessica B. Lau, Maggie C. Y. Kuloyo, Olukayode Wei, Siwen Kyin, Saw Harris, Rachel L. Onstott, Tullis C. Shwe, Henry H. van Heerden, Esta Guo, Ling Slater, Greg F. |
| Author_xml | – sequence: 1 givenname: Maggie C. Y. surname: Lau fullname: Lau, Maggie C. Y. organization: Department of Geosciences, Princeton University, Princeton, NJ 08544 – sequence: 2 givenname: Thomas L. surname: Kieft fullname: Kieft, Thomas L. organization: Department of Biology, New Mexico Institute of Mining and Technology, Socorro, NM 87801 – sequence: 3 givenname: Olukayode surname: Kuloyo fullname: Kuloyo, Olukayode organization: Department of Microbial, Biochemical, and Food Biotechnology, University of the Free State, Bloemfontein 9301, South Africa – sequence: 4 givenname: Borja surname: Linage-Alvarez fullname: Linage-Alvarez, Borja organization: Department of Microbial, Biochemical, and Food Biotechnology, University of the Free State, Bloemfontein 9301, South Africa – sequence: 5 givenname: Esta surname: van Heerden fullname: van Heerden, Esta organization: Department of Microbial, Biochemical, and Food Biotechnology, University of the Free State, Bloemfontein 9301, South Africa – sequence: 6 givenname: Melody R. surname: Lindsay fullname: Lindsay, Melody R. organization: Department of Geosciences, Princeton University, Princeton, NJ 08544 – sequence: 7 givenname: Cara surname: Magnabosco fullname: Magnabosco, Cara organization: Department of Geosciences, Princeton University, Princeton, NJ 08544 – sequence: 8 givenname: Wei surname: Wang fullname: Wang, Wei organization: High Throughput Sequencing and Microarray Facility, Lewis–Sigler Institute for Integrative Genomics, Princeton University, NJ 08544 – sequence: 9 givenname: Jessica B. surname: Wiggins fullname: Wiggins, Jessica B. organization: High Throughput Sequencing and Microarray Facility, Lewis-Sigler Institute for Integrative Genomics, Princeton University, NJ 08544 – sequence: 10 givenname: Ling surname: Guo fullname: Guo, Ling organization: High Throughput Sequencing and Microarray Facility, Lewis-Sigler Institute for Integrative Genomics, Princeton University, NJ 08544 – sequence: 11 givenname: David H. surname: Perlman fullname: Perlman, David H. organization: Proteomics and Mass Spectrometry Core, Department of Molecular Biology, Princeton University, NJ 08544 – sequence: 12 givenname: Saw surname: Kyin fullname: Kyin, Saw organization: Proteomics and Mass Spectrometry Core, Department of Molecular Biology, Princeton University, NJ 08544 – sequence: 13 givenname: Henry H. surname: Shwe fullname: Shwe, Henry H. organization: Proteomics and Mass Spectrometry Core, Department of Molecular Biology, Princeton University, NJ 08544 – sequence: 14 givenname: Rachel L. surname: Harris fullname: Harris, Rachel L. organization: Department of Geosciences, Princeton University, Princeton, NJ 08544 – sequence: 15 givenname: Youmi surname: Oh fullname: Oh, Youmi organization: Atmospheric and Oceanic Sciences, Princeton University, Princeton, NJ 08544 – sequence: 16 givenname: Min Joo surname: Yi fullname: Yi, Min Joo organization: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544 – sequence: 17 givenname: Roland surname: Purtschert fullname: Purtschert, Roland organization: Climate and Environmental Physics, Physics Institute, University of Bern, 3012 Bern, Switzerland – sequence: 18 givenname: Greg F. surname: Slater fullname: Slater, Greg F. organization: School of Geography and Earth Sciences, McMaster University, Hamilton, ON, Canada L8S 4K1 – sequence: 19 givenname: Shuhei surname: Ono fullname: Ono, Shuhei organization: Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139 – sequence: 20 givenname: Siwen surname: Wei fullname: Wei, Siwen organization: Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E3 – sequence: 21 givenname: Long surname: Li fullname: Li, Long organization: Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E3 – sequence: 22 givenname: Barbara Sherwood surname: Lollar fullname: Lollar, Barbara Sherwood organization: Department of Earth Sciences, University of Toronto, Toronto, ON, Canada M5S 3B1 – sequence: 23 givenname: Tullis C. surname: Onstott fullname: Onstott, Tullis C. organization: Department of Geosciences, Princeton University, Princeton, NJ 08544 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27872277$$D View this record in MEDLINE/PubMed |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: M.C.Y.L. and T.C.O. designed research; M.C.Y.L., C.M., W.W., and T.C.O. planned the technical approach of metatranscriptomics; M.C.Y.L., D.H.P., and T.C.O. planned the technical approach of metaproteomics; M.C.Y.L., T.L.K., O.K., B.L.-A., E.v.H., M.R.L., C.M., W.W., J.B.W., L.G., D.H.P., S.K., H.H.S., R.P., G.F.S., S.O., S.W., L.L., B.S.L., and T.C.O. performed research; E.v.H. was the point of contact with the mining company; M.C.Y.L., T.L.K., O.K., B.L.-A., E.v.H., M.R.L., and C.M. collected samples; M.C.Y.L., M.R.L., R.L.H., Y.O., M.J.Y., R.P., G.F.S., S.O., S.W., L.L., B.S.L., and T.C.O. analyzed data; G.F.S., S.O., L.L., B.S.L., and T.C.O. assisted with the interpretation of isotopic data; T.L.K., C.M., W.W., J.B.W., D.H.P., S.K., G.F.S., L.L., B.S.L., and T.C.O. contributed to and/or commented on the earlier drafts of the manuscript; and M.C.Y.L. wrote the paper. 5Present address: Simons Center for Data Analysis, Simons Foundation, New York, NY 10010. 6Present address: Department of Chemistry, Princeton University, NJ 08544. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved October 26, 2016 (received for review August 10, 2016) 7Present address: Department of Earth, Atmospheric, and Planetary Sciences, Purdue University, West Lafayette, IN 47907. 2Present address: Energy Bioengineering and Geomicrobiology Group, University of Calgary, Calgary, AB, Canada T2N 1N4. 3Present address: Consorcio de Promoción del Ovino, 49630 Villalpando, Castillo-León, Spain. 4Present address: Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717. |
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| Snippet | Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H₂. Methanogens and sulfate reducers, and... Microorganisms are known to live in the deep subsurface, kilometers below the photic zone, but the community-wide metabolic networks and trophic structures... Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H Methanogens and sulfate reducers, and the... Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H^sub 2^. Methanogens and sulfate reducers,... Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H2 Methanogens and sulfate reducers, and the... |
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| SubjectTerms | Autotrophic Processes Biological Sciences Carbon - metabolism Denitrification Ecosystem Environmental conditions Metabolism Methane - biosynthesis Microbiota Microorganisms Nitrogen - metabolism PNAS Plus South Africa Sulfates Sulfur Sulfur - metabolism Thermodynamics |
| Title | An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers |
| URI | https://www.jstor.org/stable/26472793 https://www.ncbi.nlm.nih.gov/pubmed/27872277 https://www.proquest.com/docview/1848086860 https://www.proquest.com/docview/1842599931 https://pubmed.ncbi.nlm.nih.gov/PMC5150411 |
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