An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers
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Lau-2016-An oligotrophic deep-subsurface commu.pdf
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Author(s)
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
Date Issued
November 2016
Journal
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences (U.S.)
Citation
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
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Final published version
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.
MIT Department
Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
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DOI of Published Version
https://doi.org/10.1073/pnas.1612244113
