Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes; Qian, Chen; Xiong, Weili; Hettich, Robert L.; Frutschi, Manon; Bernier-Latmani, Rizlan

doi:10.1038/s41396-022-01207-w

Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

Journal Article · Wed Feb 16 00:00:00 EST 2022 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-022-01207-w· OSTI ID:1845369

; ; Alneberg, Johannes; Qian, Chen; ; ; Frutschi, Manon;

Abstract

Microbial life is widespread in the terrestrial subsurface and present down to several kilometers depth, but the energy sources that fuel metabolism in deep oligotrophic and anoxic environments remain unclear. In the deep crystalline bedrock of the Fennoscandian Shield at Olkiluoto, Finland, opposing gradients of abiotic methane and ancient seawater-derived sulfate create a terrestrial sulfate-methane transition zone (SMTZ). We used chemical and isotopic data coupled to genome-resolved metaproteogenomics to demonstrate active life and, for the first time, provide direct evidence of active anaerobic oxidation of methane (AOM) in a deep terrestrial bedrock. Proteins from Methanoperedens (formerly ANME-2d) are readily identifiable despite the low abundance (≤1%) of this genus and confirm the occurrence of AOM. This finding is supported by 13C-depleted dissolved inorganic carbon. Proteins from Desulfocapsaceae and Desulfurivibrionaceae, in addition to 34S-enriched sulfate, suggest that these organisms use inorganic sulfur compounds as both electron donor and acceptor. Zerovalent sulfur in the groundwater may derive from abiotic rock interactions, or from a non-obligate syntrophy with Methanoperedens, potentially linking methane and sulfur cycles in Olkiluoto groundwater. Finally, putative episymbionts from the candidate phyla radiation (CPR) and DPANN archaea represented a significant diversity in the groundwater (26/84 genomes) with roles in sulfur and carbon cycling. Our results highlight AOM and sulfur disproportionation as active metabolisms and show that methane and sulfur fuel microbial activity in the deep terrestrial subsurface.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1845369

Alternate ID(s):: OSTI ID: 1883769

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 6 Vol. 16; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Journal Article · Mon Feb 10 19:00:00 EST 2020 · The ISME Journal · OSTI ID:1606636

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59 BASIC BIOLOGICAL SCIENCES

Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

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