Microbial Resuscitation and Growth Rates in Deep Permafrost: Lipid Stable Isotope Probing Results from the Permafrost Research Tunnel in Fox, Alaska

Abstract

Permafrost is at increasing risk of thaw as cold regions in the Northern Hemisphere continue to warm. Of particular concern is ice-rich, organic-rich, syngenetic "yedoma" type permafrost. The lability of organic carbon in permafrost post-thaw largely depends on the rate at which microorganisms resuscitate and proliferate after thousands of years in below-freezing, dark, anaerobic conditions. However, the resuscitation and growth rates of microorganisms in deep permafrost are unknown. To quantify these rates, we conducted lipid stable isotope probing (lipid-SIP) on permafrost cores collected from four locations within the Permafrost Tunnel near Fairbanks, Alaska. We compare rates of microbial growth, marker gene sequences, and greenhouse gas (CO2, CH4) emissions across cores held anaerobically at ambient and elevated temperatures. In deep, ancient permafrost, microbial biomass turnover is exceedingly slow, often undetectable, within the first month following thaw. Our results indicate microbial growth in response to anaerobic thaw has a notable lag period, where only 0.001 - 0.01% of cells turn over per day. This suggests a slow reawakening that could provide some buffer between anomalous warmth and C degradation if permafrost refreezes seasonally. However, within six months, microbial communities undergo dramatic restructuring and succession, producing communities that are distinct from both the emplaced ancient and overlying surface communities. These results have critical implications for predictions of microbial biogeochemical contributions in a warming arctic, especially as thaw proceeds into deeper and more ancient permafrost horizons. Plain Language SummaryPermafrost, earth material like soil, rock, or ice continually frozen for more than two years, contains more organic carbon than is currently in the atmosphere as CO2. As the Arctic warms and permafrost thaws, ancient microbes can reactivate, allowing the degradation of organic carbon that has accumulated in permafrost over millenia, resulting in the release of greenhouse gases. In this work, we measured the rates at which permafrost microorganisms resuscitate during thaw and related these growth rates to changes in microbial community composition and greenhouse gas emissions. Key PointsO_LIMicrobial growth is extremely slow within the first 30 days of thaw. Temperature may drive which taxa are active, but not growth rates. C_LIO_LISubsurface microbes show a preference for glycolipids over phospholipids, suggesting a possible cryotolerance adaptation. C_LIO_LIAncient, entrapped gases may be the primary source of emissions in early thaw stages. C_LI