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

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.

Revisiting the Engineering Roadmap of Nitrate/Nitrite-Dependent Anaerobic Methane Oxidation

“…51,52 Candidatus M. nitroreducens, affiliated with a distinct subgroup of ANME-2d, has generally inhabited freshwater systems where nitrate is adequate (Figure 5b). 26,53,54 ANME-2d was previously found related to sulfatedependent AOM in lake sediments. 55 But the absence of genes for dissimilatory sulfate reduction impedes ANME-2d to perform sulfate reduction by itself.…”

“…The sulfate-dependent AOM is an important microbial metabolism that forms an important link between global carbon and sulfur cycles. As sulfate is the most abundant alternate terminal electron acceptor in the ocean, sulfate-dependent AOM is the dominant methane sink within marine sediments and accounts for 90% of methane emission emitted from the ocean bed. , This process is generally considered mediated by consortia of anaerobic methanotrophic archaea (ANME-1, ANME-2a/b/c, and ANME-3) in syntropy with sulfate-reducing bacteria (SRB) (Figure a). , Candidatus M. nitroreducens, affiliated with a distinct subgroup of ANME-2d, has generally inhabited freshwater systems where nitrate is adequate (Figure b). ,, ANME-2d was previously found related to sulfate-dependent AOM in lake sediments . But the absence of genes for dissimilatory sulfate reduction impedes ANME-2d to perform sulfate reduction by itself.…”

Thermodynamic Inhibition of Microbial Sulfur Disproportionation in a Multisubunit Designed Sulfur-Siderite Packed Bioreactor

“…They were further enriched during the S 0 DP period, possibly due to the release of soluble microbial products from decaying cells. − Afterward, the heterotrophs were significantly reduced after aeration due to the sufficient oxidation of biodegradable organics. Due to the limited identification of SDBs (Figure D), the top 13 genera belonging to Desulfocapsaceae were identified, exhibiting S 0 DP function . The highest percentage of total SDBs (3.0%), mainly contributed by Desulfocapsa , unexpectedly appeared in the S 0 AD period, possibly originating from some dead zones with SHEAs exhaustion.…”

Giant genes are rare but implicated in cell wall degradation by predatory bacteria

“…The public datasets in which giant proteins were detected were from landfill leachate metagenomes (Grégoire et al 2023) , anaerobic digester sludge in the United States (Mei and Liu 2022) and China (Liu et al 2021) , lake water in Spain (Cabello-Yeves et al 2022) and Finland (Buck et al 2021) , subsurface fracture fluids (Casar et al 2021) in the United States, groundwater in New Zealand (Mosley et al 2022) and Finland (Bell et al 2022) , hydrocarbon field communities in Canada (An et al 2013) , Norwegian fjord waters (Suarez et al 2022) , river estuary sediment from China (Wang et al 2021) , magnetotactic enrichment communities (Lin et al 2020) , and a limonene enrichment from bog soil in Germany (Kizina et al 2022).…”