| Abstract: |
Permafrost is at increasing risk of thaw as cold regions in the Northern Hemisphere continue to warm. The lability of organic carbon in permafrost post‐taw largely depends on the rate at which microorganisms resuscitate and proliferate after many years in freezing, dark, anaerobic conditions. Moreover, the bulk of the Earth's permafrost exists at deep subsurface horizons, far below the active layer, that have been isolated for hundreds, thousands, or millions of years. However, the resuscitation and growth rates of microorganisms in deep permafrost remain unknown. To quantify these rates, we conducted lipid stable isotope probing (lipid‐SIP) on permafrost cores of late‐pleistocene age from four locations within the Permafrost Research 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 (−4°C) and elevated temperatures (4°C, 12°C). In deep, ancient permafrost, microbial growth is exceedingly slow, often undetectable, within the first month following thaw, indicating 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 but remains anaerobic. However, within 6 months, microbial communities undergo dramatic restructuring and become distinct from both the 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 Summary: Permafrost, frozen earth material containing soil, rock, and ice, harbors 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. We find that microbes in thawing subsurface permafrost exhibit a slow "reawakening" at first, but within 6 months the microbial community undergoes dramatic changes. Microbial communities that survive and proliferate after burial for thousands of years do not resemble those on the surface and exhibit reduced diversity. Finally, we note that microbes in subsurface permafrost rely on different kinds of lipids to construct their cell membranes: these compounds may have helped them survive freezing, dark conditions for millenia. Key Points: Microbial growth is extremely slow within the first 30 days of thaw. Temperature may drive which taxa are active, but not growth ratesSubsurface microbes preferentially produce glycolipids over phospholipids, suggesting a role in cryotoleranceAncient, entrapped gases may be the primary source of emissions in early thaw stages [ABSTRACT FROM AUTHOR] |