Climate change is rapidly transforming Arctic landscapes where increasing soil temperatures speed up permafrost thaw. This exposes large carbon stocks to microbial decomposition, possibly worsening climate change by releasing more greenhouse gases. Understanding how microbes break down soil carbon, especially under the anaerobic conditions of thawing permafrost, is important to determine future changes. Here, we studied the microbial community dynamics and soil carbon decomposition potential in permafrost and active layer soils under anaerobic laboratory conditions that simulated an Arctic summer thaw. The microbial and viral compositions in the samples were analyzed based on metagenomes, metagenome-assembled genomes, and metagenomic viral contigs (mVCs). Following the thawing of permafrost, there was a notable shift in microbial community structure, with fermentative Firmicutes and Bacteroidota taking over from Actinobacteria and Proteobacteria over the 60-day incubation period. The increase in iron and sulfate-reducing microbes had a significant role in limiting methane production from thawed permafrost, underscoring the competition within microbial communities. We explored the growth strategies of microbial communities and found that slow growth was the major strategy in both the active layer and permafrost. Our findings challenge the assumption that fast-growing microbes mainly respond to environmental changes like permafrost thaw. Instead, they indicate a common strategy of slow growth among microbial communities, likely due to the thermodynamic constraints of soil substrates and electron acceptors, and the need for microbes to adjust to post-thaw conditions. The mVCs harbored a wide range of auxiliary metabolic genes that may support cell protection from ice formation in virus-infected cells.IMPORTANCE As the Arctic warms, thawing permafrost unlocks carbon, potentially accelerating climate change by releasing greenhouse gases. Our research delves into the underlying biogeochemical processes likely mediated by the soil microbial community in response to the wet and anaerobic conditions, akin to an Arctic summer thaw. We observed a significant shift in the microbial community post-thaw, with fermentative bacteria like Firmicutes and Bacteroidota taking over and switching to different fermentation pathways. The dominance of iron and sulfate-reducing bacteria likely constrained methane production in the thawing permafrost. Slow-growing microbes outweighed fast-growing ones, even after thaw, upending the expectation that rapid microbial responses to dominate after permafrost thaws. This research highlights the nuanced and complex interactions within Arctic soil microbial communities and underscores the challenges in predicting microbial response to environmental change. As the Arctic warms, thawing permafrost unlocks carbon, potentially accelerating climate change by releasing greenhouse gases. Our research delves into the underlying biogeochemical processes likely mediated by the soil microbial community in response to the wet and anaerobic conditions, akin to an Arctic summer thaw. We observed a significant shift in the microbial community post-thaw, with fermentative bacteria like Firmicutes and Bacteroidota taking over and switching to different fermentation pathways. The dominance of iron and sulfate-reducing bacteria likely constrained methane production in the thawing permafrost. Slow-growing microbes outweighed fast-growing ones, even after thaw, upending the expectation that rapid microbial responses to dominate after permafrost thaws. This research highlights the nuanced and complex interactions within Arctic soil microbial communities and underscores the challenges in predicting microbial response to environmental change.

Warming temperatures in continuous permafrost zones of the Arctic will alter both hydrological and geochemical soil conditions, which are strongly linked with heterotrophic microbial carbon (C) cycling. Heterogeneous permafrost landscapes are often dominated by polygonal features formed by expanding ice wedges: water accumulates in low centered polygons (LCPs), and water drains outward to surrounding troughs in high centered polygons (HCPs). These geospatial differences in hydrology cause gradients in biogeochemistry, soil C storage potential, and thermal properties. Presently, data quantifying carbon dioxide (CO2) and methane (CH4) release from HCP soils are needed to support modeling and evaluation of warming-induced CO2 and CH4 fluxes from tundra soils. This study quantifies the distribution of microbial CO2 and CH4 release in HCPs over a range of temperatures and draws comparisons to previous LCP studies. Arctic tundra soils were initially characterized for geochemical and hydraulic properties. Laboratory incubations at -2, +4, and +8 degrees C were used to quantify temporal trends in CO2 and CH4 production from homogenized active layer organic and mineral soils in HCP centers and troughs, and methanogen abundance was estimated from mcrA gene measurements. Results showed that soil water availability, organic C, and redox conditions influence temporal dynamics and magnitude of gas production from HCP active layer soils during warming. At early incubation times (2-9 days), higher CO2 emissions were observed from HCP trough soils than from HCP center soils, but increased CO2 production occurred in center soils at later times (>20 days). HCP center soils did not support methanogenesis, but CH4-producing trough soils did indicate methanogen presence. Consistent with previous LCP studies, HCP organic soils showed increased CO2 and CH4 production with elevated water content, but HCP trough mineral soils produced more CH4 than LCP mineral soils. HCP mineral soils also released substantial CO2 but did not show a strong trend in CO2 and CH4 release with water content. Knowledge of temporal and spatial variability in microbial C mineralization rates of Arctic soils in response to warming are key to constraining uncertainties in predictive climate models.

Decomposition of soil organic matter (SOM) in permafrost terrain and the production of greenhouse gases is a key factor for understanding climate change-carbon feedbacks. Previous studies have shown that SOM decomposition is mostly controlled by soil temperature, soil moisture, and carbon-nitrogen ratio (C:N). However, focus has generally been on site-specific processes and little is known about variations in the controls on SOM decomposition across Arctic sites. For assessing SOM decomposition, we retrieved 241 samples from 101 soil profiles across three contrasting Arctic regions and incubated them in the laboratory under aerobic conditions. We assessed soil carbon losses (C-loss) five times during a 1year incubation. The incubated material consisted of near-surface active layer (AL(NS)), subsurface active layer (AL(SS)), peat, and permafrost samples. Samples were analyzed for carbon, nitrogen, water content, C-13, N-15, and dry bulk density (DBD). While no significant differences were observed between total AL(SS) and permafrost C-loss over 1year incubation (2.32.4% and 2.51.5% C-loss, respectively), AL(NS) samples showed higher C-loss (7.94.2%). DBD was the best explanatory parameter for active layer C-loss across sites. Additionally, results of permafrost samples show that C:N ratio can be used to characterize initial C-loss between sites. This data set on the influence of abiotic parameter on microbial SOM decomposition can improve model simulations of Arctic soil CO2 production by providing representative mean values of CO2 production rates and identifying standard parameters or proxies for upscaling potential CO2 production from site to regional scales.