Patterns of permafrost microbial functional genes and in situ greenhouse gas concentrations indicate that permafrost is an active microbial ecosystem

Widespread permafrost thaw is expected to occur this century with potentially large releases of greenhouse gases including CO2, CH4, and N2O. Much of the permafrost in interior Alaska (AK) is within a few degrees of thaw (0 °C), allowing for a significant fraction of the permafrost volume to contain liquid water. As such, microorganisms inhabiting permafrost have the capacity to be active and produce greenhouse gases while permafrost is still intact (below 0 °C). We hypothesize that as permafrost approaches thaw, we should expect increases in permafrost liquid water content and microbial activities. We examined in situ permafrost water content and greenhouse gases seasonally and at multiple depths across a gradient from colder intact permafrost to warmer degrading permafrost at the Alaska Peatland Experiment (APEX) in interior AK. We installed gas probes and thermistors at 1.2, 1.8 and 2.4 m depths, co-located with boreholes for vertical nuclear magnetic resonance (NMR) to quantify in situ permafrost unfrozen water content down to 2 m. We also examined the relative abundance of genes associated with fermentation, methanogenesis, methane oxidation, and nitrous oxide production using metagenomic techniques. Permafrost temperatures ranged from -0.2 to -1.2 °C, permafrost unfrozen water content ranged from zero to 20%, and permafrost greenhouse gas concentrations ranged from 0.2 - 37% CO2, 0 - 30% CH4, and 0-300 ppm N2O. Greenhouse gas concentrations increased with depth, were seasonally dynamic, and were indicative of CO2 reduction, methanogenesis, and denitrification occurring in situ as permafrost approached thaw. The relative abundance of functional genes associated with decomposition, fermentation, N fixation, methanogenesis, sulfate reduction, and the decomposition of C1 compounds in permafrost all increased with warming permafrost. Multiple regression analysis indicated that the concentration of in situ permafrost greenhouse gases could best be explained by a combination of in situ permafrost temperature and relevant functional gene abundance. Our research indicates that intact permafrost is an active microbial ecosystem and microbial GHG producing and consuming activities occur in permafrost prior to thaw.