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.
| Original language | English |
|---|---|
| Pages (from-to) | 1583-1593 |
| Number of pages | 11 |
| Journal | ISME Journal |
| Volume | 16 |
| Issue number | 6 |
| DOIs | |
| State | Published - Jun 2022 |
Funding
We thank POSIVA OY for providing the funding and the logistical support to carry out the work, Maarit Yli-Kaila and Raila Viitala for support and assistance conducting fieldwork, Louise Balmer and Guillaume Sommer for assistance collecting samples, and Petteri Pitkänen for valuable discussions. Support for metagenomic sequencing was provided by The Census of Deep Life within the Deep Carbon Observatory and the U.S. Department of Energy Joint Genome Institute. The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. The metagenomic computations were performed on resources provided by SNIC through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX). We thank POSIVA OY for providing the funding and the logistical support to carry out the work, Maarit Yli-Kaila and Raila Viitala for support and assistance conducting fieldwork, Louise Balmer and Guillaume Sommer for assistance collecting samples, and Petteri Pitkänen for valuable discussions. Support for metagenomic sequencing was provided by The Census of Deep Life within the Deep Carbon Observatory and the U.S. Department of Energy Joint Genome Institute. The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. The metagenomic computations were performed on resources provided by SNIC through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX). Conceptualization—EB, TL, and RB-L; Methodology—EB, TL, RB-L, MF, JA, and RLH; Formal analysis—EB, Investigation—EB, MF, CQ, WX; Resources—RB-L, TL, and RLH; Writing – Original Draft—EB, and RB-L, Writing – Review and Editing—All authors; Supervision—RB-L and TL, Funding acquisition—RB-L and TL.
| Funders | Funder number |
|---|---|
| SNIC | |
| U.S. Department of Energy Joint Genome Institute | |
| Office of Science | DE-AC02-05CH11231 |