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.

Arctic permafrost soils store substantial reserves of organic matter (OM) from which microbial transformation contributes significantly to greenhouse gas emissions of CH4 and CO2. However, many younger sediments exposed by glacier retreat and sea level change in fjord landscapes lack significant organic carbon resources, so their capacity to promote greenhouse gas emissions is unclear. We therefore studied the effects of increased temperatures (4 degrees C and 21 degrees C) and OM on rates of Fe(III) reduction, CO2 production, and methanogenesis in three different Holocene sedimentary units from a single site within the former marine limit of Adventdalen, Svalbard. Higher temperature and OM addition generally stimulated CH4 production and CO2 production and an increase in Bacteria and Archaea abundance in all units, whereas an equal stimulation of Fe(II) production by OM amendment and an increase in temperature to 21 degrees C was only observed in a diamicton. We observed an accumulation of Fe(II) in beach and delta deposits as well but saw no stimulating effect of additional OM or increased temperature. Interestingly, we observed a small but significant production of CH4 in all units despite the presence of large reservoirs of Fe(III), sulfate, and nitrate, indicating either the availability of substrates that are primarily used by methanogens or a tight physical coupling between fermentation and methanogenesis by direct electron transfer. Our study clearly illustrates a significant challenge that comes with the large heterogeneity on a narrow spatial scale that one encounters when studying soils that have complex histories.