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With rising global temperatures, permafrost carbon stores are vulnerable to microbial degradation. The enzyme latch theory states that polyphenols should accumulate in saturated peatlands due to diminished phenol oxidase activity, inhibiting resident microbes and promoting carbon stabilization. Pairing microbiome and geochemical measurements along a permafrost thaw-induced saturation gradient in Stordalen Mire, a model Arctic peatland, we confirmed a negative relationship between phenol oxidase expression and saturation but failed to support other trends predicted by the enzyme latch. To inventory alternative polyphenol removal strategies, we built CAMPER, a gene annotation tool leveraging polyphenol enzyme knowledge gleaned across microbial ecosystems. Applying CAMPER to genome-resolved metatranscriptomes, we identified genes for diverse polyphenol-active enzymes expressed by various microbial lineages under a range of redox conditions. This shifts the paradigm that polyphenols stabilize carbon in saturated soils and highlights the need to consider both oxic and anoxic polyphenol metabolisms to understand carbon cycling in changing ecosystems., (© 2024. The Author(s).)

Rapid Arctic environmental change affects the entire Earth system as thawing permafrost ecosystems release greenhouse gases to the atmosphere. Understanding how much permafrost carbon will be released, over what time frame, and what the relative emissions of carbon dioxide and methane will be is key for understanding the impact on global climate. In addition, the response of vegetation in a warming climate has the potential to offset at least some of the accelerating feedback to the climate from permafrost carbon. Temperature, organic carbon, and ground ice are key regulators for determining the impact of permafrost ecosystems on the global carbon cycle. Together, these encompass services of permafrost relevant to global society as well as to the people living in the region and help to determine the landscape-level response of this region to a changing climate. [ABSTRACT FROM AUTHOR]

Permafrost thaw could induce substantial carbon (C) emissions to the atmosphere, and thus trigger a positive feedback to climate warming. As the engine of biogeochemical cycling, soil microorganisms exert a critical role in mediating the direction and strength of permafrost C‐climate feedback. However, our understanding about the impacts of thermokarst (abrupt permafrost thaw) on microbial structure and function remains limited. Here we employed metagenomic sequencing to analyze changes in topsoil (0–15 cm) microbial communities and functional genes along a permafrost thaw sequence (1, 10, and 16 years since permafrost collapse) on the Tibetan Plateau. By combining laboratory incubation and a two‐pool model, we then explored changes in soil labile and stable C decomposition along the thaw sequence. Our results showed that topsoil microbial α‐diversity decreased, while the community structure and functional gene abundance did not exhibit any significant change at the early stage of collapse (1 year since collapse) relative to non‐collapsed control. However, as the time since the collapse increased, both the topsoil microbial community structure and functional genes differed from the control. Abundances of functional genes involved in labile C degradation decreased while those for stable C degradation increased at the late stage of collapse (16 years since collapse), largely driven by changes in substrate properties along the thaw sequence. Accordingly, faster stable C decomposition occurred at the late stage of collapse compared to the control, which was associated with the increase in relative abundance of functional genes for stable C degradation. These results suggest that upland thermokarst alters microbial structure and function, particularly enhances soil stable C decomposition by modulating microbial functional genes, which could reinforce a warmer climate over the decadal timescale. [ABSTRACT FROM AUTHOR]

Accelerating permafrost thaw across high-latitude ecosystems increases organic matter (OM) availability to soil microorganisms. The chemical composition of permafrost-derived OM, which influences microbial metabolic efficiency, may determine whether the Arctic remains a critical carbon sink in the future or shifts to net a source of greenhouse gases. During a 90-day, simulated thaw experiment, we measured shifts in the chemistry of soil and dissolved organic matter pools sourced from surface (0–10 cm) and subsurface (16–25 cm) permafrost layers. We manipulated temperature (1 versus 15 °C) and redox (drained versus saturated) to mimic field-relevant conditions and tested whether variability in OM chemistry could be explained by the activities of six hydrolytic enzymes that catalyze carbon, nitrogen, and phosphorus mineralization. We found that permafrost depth and enzyme activities were significantly correlated with shifts in soil OM (SOM) functional group chemistries, as measured by diffuse reflectance infrared Fourier transform (DRIFT) spectroscopy. Greater variability in dissolved OM (DOM) chemistries were driven by redox and pH. Our results suggest depth-resolved analyses of permafrost vulnerability to enzymatic hydrolysis may help explain distinct patterns in SOM versus DOM cycling that can be used to constrain modeled projections of Arctic carbon storage during global change. • Hydrolytic enzymes strongly influenced permafrost soil organic matter chemistry. • Redox and pH explained shifts in dissolved organic matter chemistry. • DRIFT-detectable functional bands are early indicators of permafrost decomposition. • Different pathways of SOM versus DOM mineralization may influence Arctic C storage. [ABSTRACT FROM AUTHOR]