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ABSTRACT Permafrost microbial research has flourished in the past decades, due in part to improvements in sampling and molecular techniques, but also the increased focus on the permafrost greenhouse gas feedback to climate change and other ecological processes in high latitude and alpine permafrost soils. Permafrost microorganisms are adapted to these extreme environments and remain active at low temperatures and when resources are limited. They are also an important component of global elemental cycles as they regulate organic matter turnover and greenhouse gas production, particularly as permafrost thaws. Here we review the permafrost microbiology literature coupled with an exploration of its historical aspects, with a particular focus on a new understanding advanced by molecular biology techniques. We further identify knowledge gaps and ways forward to improve our understanding of microbial contributions to ecosystem biogeochemistry of permafrost‐affected systems. 

Abstract Nitrogen regulates multiple aspects of the permafrost climate feedback, including plant growth, organic matter decomposition, and the production of the potent greenhouse gas nitrous oxide. Despite its importance, current estimates of permafrost nitrogen are highly uncertain. Here, we compiled a dataset of >2000 samples to quantify nitrogen stocks in the Yedoma domain, a region with organic-rich permafrost that contains ~25% of all permafrost carbon. We estimate that the Yedoma domain contains 41.2 gigatons of nitrogen down to ~20 metre for the deepest unit, which increases the previous estimate for the entire permafrost zone by ~46%. Approximately 90% of this nitrogen (37 gigatons) is stored in permafrost and therefore currently immobile and frozen. Here, we show that of this amount, ¾ is stored >3 metre depth, but if partially mobilised by thaw, this large nitrogen pool could have continental-scale consequences for soil and aquatic biogeochemistry and global-scale consequences for the permafrost feedback. 

Abstract Tundra and boreal ecosystems encompass the northern circumpolar permafrost region and are experiencing rapid environmental change with important implications for the global carbon (C) budget. We analysed multi-decadal time series containing 302 annual estimates of carbon dioxide (CO₂) flux across 70 permafrost and non-permafrost ecosystems, and 672 estimates of summer CO₂flux across 181 ecosystems. We find an increase in the annual CO₂sink across non-permafrost ecosystems but not permafrost ecosystems, despite similar increases in summer uptake. Thus, recent non-growing-season CO₂losses have substantially impacted the CO₂balance of permafrost ecosystems. Furthermore, analysis of interannual variability reveals warmer summers amplify the C cycle (increase productivity and respiration) at putatively nitrogen-limited sites and at sites less reliant on summer precipitation for water use. Our findings suggest that water and nutrient availability will be important predictors of the C-cycle response of these ecosystems to future warming. 

Abstract The northern permafrost region has been projected to shift from a net sink to a net source of carbon under global warming. However, estimates of the contemporary net greenhouse gas (GHG) balance and budgets of the permafrost region remain highly uncertain. Here, we construct the first comprehensive bottom‐up budgets of CO₂, CH₄, and N₂O across the terrestrial permafrost region using databases of more than 1000 in situ flux measurements and a land cover‐based ecosystem flux upscaling approach for the period 2000–2020. Estimates indicate that the permafrost region emitted a mean annual flux of 12 (−606, 661) Tg CO₂–C yr⁻¹, 38 (22, 53) Tg CH₄–C yr⁻¹, and 0.67 (0.07, 1.3) Tg N₂O–N yr⁻¹to the atmosphere throughout the period. Thus, the region was a net source of CH₄and N₂O, while the CO₂balance was near neutral within its large uncertainties. Undisturbed terrestrial ecosystems had a CO₂sink of −340 (−836, 156) Tg CO₂–C yr⁻¹. Vertical emissions from fire disturbances and inland waters largely offset the sink in vegetated ecosystems. When including lateral fluxes for a complete GHG budget, the permafrost region was a net source of C and N, releasing 144 (−506, 826) Tg C yr⁻¹and 3 (2, 5) Tg N yr⁻¹. Large uncertainty ranges in these estimates point to a need for further expansion of monitoring networks, continued data synthesis efforts, and better integration of field observations, remote sensing data, and ecosystem models to constrain the contemporary net GHG budgets of the permafrost region and track their future trajectory. 

Abstract The physical and chemical changes that accompany permafrost thaw directly influence the microbial communities that mediate the decomposition of formerly frozen organic matter, leading to uncertainty in permafrost–climate feedbacks. Although changes to microbial metabolism and community structure are documented following thaw, the generality of post‐thaw assembly patterns across permafrost soils of the world remains uncertain, limiting our ability to predict biogeochemistry and microbial community responses to climate change. Based on our review of the Arctic microbiome, permafrost microbiology, and community ecology, we propose thatAssembly Theoryprovides a framework to better understand thaw‐mediated microbiome changes and the implications for community function and climate feedbacks. This framework posits that the prevalence of deterministic or stochastic processes indicates whether the community is well‐suited to thrive in changing environmental conditions. We predict that on a short timescale and following high‐disturbance thaw (e.g., thermokarst), stochasticity dominates post‐thaw microbiome assembly, suggesting that functional predictions will be aided by detailed information about the microbiome. At a longer timescale and lower‐intensity disturbance (e.g., active layer deepening), deterministic processes likely dominate, making environmental parameters sufficient for predicting function. We propose that the contribution of stochastic and deterministic processes to post‐thaw microbiome assembly depends on the characteristics of the thaw disturbance, as well as characteristics of the microbial community, such as the ecological and phylogenetic breadth of functional guilds, their functional redundancy, and biotic interactions. These propagate across space and time, potentially providing a means for predicting the microbial forcing of greenhouse gas feedbacks to global climate change.