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.; Ono, Shuhei; Wei, Siwen; ... (2016). An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers. Proceedings of the National Academy of Sciences of the United States of America - PNAS, 113(49), E7927-E7936. National Academy of Sciences NAS 10.1073/pnas.1612244113

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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, overcomen thermodynamic barriers imposed by the environmental conditions in the deep subsurface.

Item Type:

Journal Article (Original Article)

Division/Institute:

08 Faculty of Science > Physics Institute > Climate and Environmental Physics

UniBE Contributor:

Purtschert, Roland

Subjects:

500 Science > 530 Physics

ISSN:

0027-8424

Publisher:

National Academy of Sciences NAS

Language:

English

Submitter:

Doris Rätz

Date Deposited:

16 Feb 2017 10:31

Last Modified:

16 Feb 2017 10:31

Publisher DOI:

10.1073/pnas.1612244113

PubMed ID:

27872277

BORIS DOI:

10.7892/boris.92205

URI:

https://boris.unibe.ch/id/eprint/92205

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