Redox determines greenhouse gas production kinetics and metabolic traits in water-saturated thawing permafrost peat

Redox conditions, influenced by the availability of oxygen, are expected to dictate the rate of CO₂ and CH₄ production and to shape the composition and metabolism of microbial communities. Here, we use thawing permafrost peat in thermokarst water under a gradient of initial O₂ concentrations to experimentally cover the variability in redox conditions potentially found across thawing landscapes. The three main greenhouse gases, CO₂, CH₄ and N₂O, responded differently to O₂ absence. CO₂ production along the O₂ gradient could be modeled by the Michaelis Menten equation revealing a sharp decrease when oxygen dropped under 100 μM. Under anoxic conditions CO₂ yield decreased by 98% and maximum net production rate by 85% when compared to oxic conditions during the 11 days after thaw. N₂O production was observed under anoxic conditions, while CH₄ yield and CH₄ accumulation rates did not differ across the redox gradient. The latter is due to the release of stored CH₄ due to thawing. Differences between oxic and anoxic conditions were reflected in the microbial genomic composition, with changes in taxonomic and functional groups, such as N₂O reducers, fermenters, denitrifiers and sulfur reducers increasing under anoxic conditions. Genomic changes towards less efficient central metabolism further explained the CO₂ production yields and rates limited by O₂ availability as predicted by thermodynamics. Together with the Michaelis Menten models the metabolic reconstruction pinpoint to critical thresholds of CO₂ release at suboxic conditions and thus need to be considered when explaining and modeling highly variable CO₂ emissions across thawing landscapes.