TY - JOUR
T1 - An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers
AU - Lau, Maggie C.Y.
AU - Kieft, Thomas L.
AU - Kuloyo, Olukayode
AU - Linage-Alvarez, Borja
AU - Van Heerden, Esta
AU - Lindsay, Melody R.
AU - Magnabosco, Cara
AU - Wang, Wei
AU - Wiggins, Jessica B.
AU - Guo, Ling
AU - Perlman, David H.
AU - Kyin, Saw
AU - Shwe, Henry H.
AU - Harris, Rachel L.
AU - Oh, Youmi
AU - Yi, Min Joo
AU - Purtschert, Roland
AU - Slater, Greg F.
AU - Ono, Shuhei
AU - Wei, Siwen
AU - Li, Long
AU - Lollar, Barbara Sherwood
AU - Onstott, Tullis C.
N1 - Funding Information:
This work was supported by funding from National Science Foundation [Grants EAR-0948659 and DEB-1441646 (to T.C.O.) and DGE- 1148900 (to C.M.)], the Deep Carbon Observatory (Alfred P. Sloan Foundation) [Sloan 2013-10-03, subaward 48045 (to M.C.Y.L.)], and the Center for Dark Energy Biosphere Investigations (C.M.). Partial support for isotopic analyses was provided by the Natural Sciences and Engineering Research Council of Canada (B.S.L.). This article is Center for Dark Energy Biosphere Investigations Contribution 340.
PY - 2016/12/6
Y1 - 2016/12/6
N2 - 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.
AB - 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.
KW - Active subsurface environment
KW - Inverted biomass pyramid
KW - Metabolic interactions
KW - Sulfur-driven autotrophic denitrifiers
KW - Syntrophy
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U2 - 10.1073/pnas.1612244113
DO - 10.1073/pnas.1612244113
M3 - Article
C2 - 27872277
AN - SCOPUS:85002080454
SN - 0027-8424
VL - 113
SP - E7927-E7936
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 49
ER -