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. 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.