Redox and temperature-sensitive changes in microbial communities and soil chemistry dictate greenhouse gas loss from thawed permafrost

Greenhouse gas (GHG) emissions from thawed permafrost are difficult to predict because they result from complex interactions between abiotic drivers and multiple, often competing, microbial metabolic processes. Our objective was to characterize mechanisms controlling methane (CH₄) and carbon dioxide (CO₂) production from permafrost. We simulated permafrost thaw for the length of one growing season (90 days) in oxic and anoxic treatments at 1 and 15 °C to stimulate aerobic and anaerobic respiration. We measured headspace CH₄ and CO₂ concentrations, as well as soil chemical and biological parameters (e.g. dissolved organic carbon (DOC) chemistry, microbial enzyme activity, N₂O production, bacterial community structure), and applied an information theoretic approach and the Akaike information criterion to find the best explanation for mechanisms controlling GHG flux. In addition to temperature and redox status, CH₄ production was explained by the relative abundance of methanogens, activity of non-methanogenic anaerobes, and substrate chemistry. Carbon dioxide production was explained by microbial community structure and chemistry of the DOC pool. We suggest that models of permafrost CO₂ production are refined by a holistic view of the system, where the prokaryote community structure and detailed chemistry are considered. In contrast, although CH₄ production is the result of many syntrophic interactions, these actions can be aggregated into a linear approach, where there is a single path of organic matter degradation and multiple conditions must be satisfied in order for methanogenesis to occur. This concept advances our mechanistic understanding of the processes governing anaerobic GHG flux, which is critical to understanding the impact the release of permafrost C will have on the global C cycle.