Anaerobic methane oxidizing archaea offset sediment methane concentrations in Arctic thermokarst lagoons

Abstract

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, and lipid biomarkers. We specifically assessed whether sulfate-driven anaerobic methane oxidation (S-AOM) through anaerobic methanotrophic archaea (ANMEs), common in marine sediments with constant supply of sulfate and methane, establish after thermokarst lagoon development and whether sulfate-driven ANMEs consequently oxidize CH4 that would be emitted to the water column under thermokarst lake conditions. The marine-influenced lagoon environment had fundamentally different methane-cycling microbial communities and metabolic pathways compared to the freshwater lakes, suggesting a substantial reshaping of microbial and carbon dynamics during lagoon formation. 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. 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. Non-competitive methylotrophic methanogens dominated the methanogenic community of the lakes and the lagoon, independent of porewater chemistry and depth. This potentially contributed to the high CH4 concentrations observed in all sulfate-poor sediments. Our study shows that S-AOM in lagoon sediments can effectively reduce sediment CH4 concentrations and we conclude that thermokarst lake to lagoon transitions have the potential to mitigate terrestrial methane fluxes before thermokarst lakes fully transition to a marine environment.

The Polar Fox Lagoon in Siberia harbours a community of Bathyarchaeota possessing the potential for peptide fermentation and acetogenesis

“…Sediment plugs were obtained from their edges using cut, sterile syringes and placed into sterile 15 ml falcon tubes which were kept frozen until DNA extraction. For a detailed analysis of physiochemical properties of the core samples see Yang et al (2022).…”

“…Samples for DNA extraction were selected based on the δ 13 C-CH 4 profile measured in 10 cm sections of the obtained sediment cores (Yang et al 2022). The bottom section was defined by a δ 13 C-CH 4 profile around −80, whereas the top profile showed a δ 13 C-CH 4 profile ranging between −55 and −40.…”