Rates of microbial hydrogen oxidation and sulfate reduction in Opalinus Clay rock

Bagnoud, Alexandre; Leupin, Olivier X.; Schwyn, B.; Bernier‐Latmani, Rizlan

doi:10.1016/j.apgeochem.2016.06.011

“…This is important in order to ascertain whether it is greater than the H 2 production rate from anoxic steel corrosion. Furthermore, the rate of sulfate consumption is also of interest 37 , in order to determine whether it can be consumed faster than it can be replenished, via diffusion of porewater from Opalinus Clay. If sulfate can be depleted, methanogenic conditions could take hold.…”

Section: Discussionmentioning

confidence: 99%

Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock

Bagnoud

¹

,

Chourey

²

,

Hettich

³

et al. 2016

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The Opalinus Clay formation will host geological nuclear waste repositories in Switzerland. It is expected that gas pressure will build-up due to hydrogen production from steel corrosion, jeopardizing the integrity of the engineered barriers. In an in situ experiment located in the Mont Terri Underground Rock Laboratory, we demonstrate that hydrogen is consumed by microorganisms, fuelling a microbial community. Metagenomic binning and metaproteomic analysis of this deep subsurface community reveals a carbon cycle driven by autotrophic hydrogen oxidizers belonging to novel genera. Necromass is then processed by fermenters, followed by complete oxidation to carbon dioxide by heterotrophic sulfate-reducing bacteria, which closes the cycle. This microbial metabolic web can be integrated in the design of geological repositories to reduce pressure build-up. This study shows that Opalinus Clay harbours the potential for chemolithoautotrophic-based system, and provides a model of microbial carbon cycle in deep subsurface environments where hydrogen and sulfate are present.

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“…Filters collected for protein were flash-frozen in a dry ice and ethanol mixture and stored at −80 °C. DNA was extracted using a modified phenol-chloroform method [ 11 , 38 ] and quantified with the dsDNA High Sensitivity Assay kit (Thermo Fisher Scientific) on a Qubit 3.0 Fluorometer. The total DNA concentration recovered from the 0.22 µm filters was 3–20 ng/L groundwater (Dataset S1 ).…”

Section: Methodsmentioning

confidence: 99%

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

Bell

¹

,

Lamminmäki

²

,

Alneberg

³

et al. 2022

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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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“…Filters collected for protein were flash-frozen in a dry ice and ethanol mixture and stored at −80°C. DNA was extracted using a modified phenol-chloroform method (11, 75) and quantified with the dsDNA High Sensitivity Assay kit (Thermo Fisher Scientific) on a Qubit 3.0 Fluorometer. Protein was extracted at the Oak Ridge National Laboratory (Oak Ridge, TN, United States) using previously described methods (11, 76).…”

Section: Methodsmentioning

confidence: 99%

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

Bell

¹

,

Lamminmäki

²

,

Alneberg

³

et al. 2021

Preprint

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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.Significance StatementThe deep terrestrial subsurface remains an environment in which there is limited understanding of the extant microbial metabolisms, despite its reported large contribution to the overall biomass on Earth. It is much less well studied than deep marine sediments. We show that microorganisms in the subsurface are active, and that methane and sulfur provide fuel in the oligotrophic and anoxic subsurface. We also uncover taxonomically and metabolically diverse ultra-small organisms that interact with larger host cells through surface attachment (episymbiosis). Methane and sulfur are commonly reported in terrestrial crystalline bedrock environments worldwide and the latter cover a significant proportion of the Earth’s surface. Thus, methane- and sulfur-dependent microbial metabolisms have the potential to be widespread in the terrestrial deep biosphere.

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Rates of microbial hydrogen oxidation and sulfate reduction in Opalinus Clay rock

Cited by 22 publications

References 14 publications

Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock

Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock

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

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

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