Seasonal thawing of high Arctic soils triggers selective microbial growth and predation.

Abstract

Climate warming threatens Arctic permafrost with seasonal cycles of freezing and thawing. Arctic soil microorganisms regulate carbon stocks and greenhouse gas exchanges with the atmosphere, yet their precise seasonal growth and dormancy dynamics, and their responses to permafrost thaw, are not well understood. We thawed frozen Svalbard active layer soil and traced microbial growth using DNA quantitative stable isotope probing with H₂¹⁸O. We observed temporal growth patterns resulting in distinct early (21-day) and late-stage (98-day) growing microbial populations. In particular, Acidobacteriota, Actinobacteriota, Bacteroidota, Proteobacteria, and predatory and epibiont bacterial taxa (such as those affiliated to Bdellovibrionota and Patescibacteria) were identified in the soil active layer as clades that were growing following thawing. Methane concentrations in our microcosms remained low, yet pmoA genes were ¹⁸O-labeled, indicating growth of aerobic methane-oxidizing bacteria. Approximately half of the microbial taxa detected did not grow, suggesting that Arctic soils constitute sizeable reservoirs of dormant microorganisms. Our results reveal complex and temporal microbial dormancy, growth, death, predation, and parasitism dynamics in seasonally changing Arctic soils. These processes likely regulate the exchange and storage of soil carbon across the increasingly vulnerable Arctic region.IMPORTANCEMicroorganisms play key roles in transforming soil carbon into greenhouse gases. As Arctic soils warm as a result of climate change, greater depths and expanses of permanently frozen soil are experiencing seasonal thaw. Despite the importance of active soil microorganisms in transforming soil carbon, the seasonal freezing and thawing of Arctic soils and associated dormancy and re-activation of microbial populations are not well constrained. Here, we thawed and incubated active layer (i.e., seasonally thawing) Arctic soil with a stable isotope to directly label the DNA of growing soil microorganisms. We found that half of the microbial diversity did not grow after thaw and that some groups, including the Bacteroidota and predatory bacteria, grew disproportionately. The growing microbial community shifted over time, and bacteria capable of oxidizing methane grew more after prolonged thaw. These findings highlight that dormancy, predation, and variable growth dynamics are important factors determining ecological and biogeochemical processes in thawing Arctic soil.