Thermokarst lagoons represent the transition state from a freshwater lacustrine to a marine environment, and receive little attention regarding their role for greenhouse gas production and release in Arctic permafrost landscapes. We studied the fate of methane (CH4) in sediments of a thermokarst lagoon in comparison to two thermokarst lakes on the Bykovsky Peninsula in northeastern Siberia through the analysis of sediment CH4 concentrations and isotopic signature, methane‐cycling microbial taxa, sediment geochemistry, lipid biomarkers, and network analysis. We assessed how differences in geochemistry between thermokarst lakes and thermokarst lagoons, caused by the infiltration of sulfate‐rich marine water, altered the microbial methane‐cycling community. Anaerobic sulfate‐reducing ANME‐2a/2b methanotrophs dominated the sulfate‐rich sediments of the lagoon despite its known seasonal alternation between brackish and freshwater inflow and low sulfate concentrations compared to the usual marine ANME habitat. Non‐competitive methylotrophic methanogens dominated the methanogenic community of the lakes and the lagoon, independent of differences in porewater chemistry and depth. This potentially contributed to the high CH4 concentrations observed in all sulfate‐poor sediments. CH4 concentrations in the freshwater‐influenced sediments averaged 1.34 ± 0.98 μmol g−1, with highly depleted δ13C‐CH4 values ranging from −89‰ to −70‰. In contrast, the sulfate‐affected upper 300 cm of the lagoon exhibited low average CH4 concentrations of 0.011 ± 0.005 μmol g−1 with comparatively enriched δ13C‐CH4 values of −54‰ to −37‰ pointing to substantial methane oxidation. Our study shows that lagoon formation specifically supports methane oxidizers and methane oxidation through changes in pore water chemistry, especially sulfate, while methanogens are similar to lake conditions.

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Subsea permafrost carbon pools below the Arctic shelf seas are a major unknown in the global carbon cycle. We combine a numerical model of sedimentation and permafrost evolution with simplified carbon turnover to estimate accumulation and microbial decomposition of organic matter on the pan-Arctic shelf over the past four glacial cycles. We find that Arctic shelf permafrost is a globally important long-term carbon sink storing 2822 (1518–4982) Pg OC, double the amount stored in lowland permafrost. Although currently thawing, prior microbial decomposition and organic matter aging limit decomposition rates to less than 48 Tg OC/yr (25–85) constraining emissions due to thaw and suggesting that the large permafrost shelf carbon pool is largely insensitive to thaw. We identify an urgent need to reduce uncertainty in rates of microbial decomposition of organic matter in cold and saline subaquatic environments. Large emissions of methane more likely derive from older and deeper sources than from organic matter in thawing permafrost.

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