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Microorganisms drive many aspects of organic carbon cycling in thawing permafrost soils, but the compositional trajectory of the post-thaw microbiome and its metabolic activity remain uncertain, which limits our ability to predict permafrost–climate feedbacks in a warming world. Using quantitative metabarcoding and metagenomic sequencing, we determined relative and absolute changes in microbiome composition and functional gene abundance during thaw incubations of wet sedge tundra collected from northern Alaska, USA. Organic soils from the tundra active-layer (0–50 cm), transition-zone (50–70 cm), and permafrost (70+ cm) depths were incubated under reducing conditions at 4 °C for 30 days to mimic an extended thaw duration. Following extended thaw, we found that iron (Fe)-cycling Gammaproteobacteria, specifically the heterotrophic Fe(III)-reducing Rhodoferax sp. and chemoautotrophic Fe(II)-oxidizing Gallionella sp., increased by 3–5 orders of magnitude in absolute abundance within the transition-zone and permafrost microbiomes, accounting for 65% of community abundance. We also found that the abundance of genes for Fe(III) reduction (e.g., MtrE) and Fe(II) oxidation (e.g., Cyc1) increased concurrently with genes for benzoate degradation and pyruvate metabolism, in which pyruvate is used to generate acetate that can be oxidized, along with benzoate, to CO2 when coupled with Fe(III) reduction. Gene abundance for CH4 metabolism decreased following extended thaw, suggesting dissimilatory Fe(III) reduction suppresses acetoclastic methanogenesis under reducing conditions. Our genomic evidence indicates that microbial carbon degradation is dominated by iron redox metabolism via an increase in gene abundance associated with Fe(III) reduction and Fe(II) oxidation during initial permafrost thaw, likely increasing microbial respiration while suppressing methanogenesis in wet sedge tundra.

 

Once thawed, up to 15% of the ∼1,000 Pg of organic carbon (C) in arctic permafrost soils may be oxidized to carbon dioxide (CO₂) by 2,100, amplifying climate change. However, predictions of this amplification strength ignore the oxidation of permafrost C to CO₂in surface waters (photomineralization). We characterized the wavelength dependence of permafrost dissolved organic carbon (DOC) photomineralization and demonstrate that iron catalyzes photomineralization of old DOC (4,000–6,300 a BP) derived from soil lignin and tannin. Rates of CO₂production from photomineralization of permafrost DOC are twofold higher than for modern DOC. Given that model predictions of future net loss of ecosystem C from thawing permafrost do not include the loss of CO₂to the atmosphere from DOC photomineralization, current predictions of an average of 208 Pg C loss by 2,299 may be too low by ~14%.

 

Soil anoxia is common in the annually thawed surface (‘active’) layer of permafrost soils, particularly when soils are saturated, and supports anaerobic microbial metabolism and methane (CH4) production. Rainfall contributes to soil saturation, but can also introduce oxygen, causing soil oxidation and altering anoxic conditions. We simulated a rainfall event in soil mesocosms from two dominant tundra types, tussock tundra and wet sedge tundra, to test the impacts of rainfall‐induced soil oxidation on microbial communities and their metabolic capacity for anaerobic CH4 production and aerobic respiration following soil oxidation. In both types, rainfall increased total soil O2 concentration, but in tussock tundra there was a 2.5‐fold greater increase in soil O2 compared to wet sedge tundra due to differences in soil drainage. Metagenomic and metatranscriptomic analyses found divergent microbial responses to rainfall between tundra types. Active microbial taxa in the tussock tundra community, including bacteria and fungi, responded to rainfall with a decline in gene expression for anaerobic metabolism and a concurrent increase in gene expression for cellular growth. In contrast, the wet sedge tundra community showed no significant changes in microbial gene expression from anaerobic metabolism, fermentation, or methanogenesis following rainfall, despite an initial increase in soil O2 concentration. These results suggest that rainfall induces soil oxidation and enhances aerobic microbial respiration in tussock tundra communities but may not accumulate or remain in wet sedge tundra soils long enough to induce a community‐wide shift from anaerobic metabolism. Thus, rainfall may serve only to maintain saturated soil conditions that promote CH4 production in low‐lying wet sedge tundra soils across the Arctic. 

Microbes and sunlight convert terrigenous dissolved organic matter (DOM) in surface waters to greenhouse gases. Prior studies show contrasting results about how biological and photochemical processes interact to contribute to the degradation of DOM. In this study, DOM leached from the organic layer of tundra soil was exposed to natural sunlight or kept in the dark, incubated in the dark with the natural microbial community, and analyzed for gene expression and DOM chemical composition. Microbial gene expression (metatranscriptomics) in light and dark treatments diverged substantially after 4 hours. Gene expression suggested that sunlight exposure of DOM initially stimulated microbial growth by (a) replacing the function of enzymes that degrade higher molecular weight DOM such as enzymes for aromatic carbon degradation, oxygenation, and decarboxylation, and (b) releasing low molecular weight compounds and inorganic nutrients from DOM. However, growth stimulation following sunlight exposure of DOM came at a cost. Sunlight depleted the pool of aromatic compounds that supported microbial growth in the dark treatment, ultimately causing slower growth in the light treatment over 5 days. These first measurements of microbial metatranscriptomic responses to photo-alteration of DOM provide a mechanistic explanation for how sunlight exposure of terrigenous DOM alters microbial processing and respiration of DOM. 

Hydroxyl radical (•OH) is produced in soils from oxidation of reduced iron (Fe(II)) by dissolved oxygen (O2) and can oxidize dissolved organic carbon (DOC) to carbon dioxide (CO2). Understanding the role of •OH on CO2 production in soils requires knowing whether Fe(II) production or O2 supply to soils limits •OH production. To test the relative importance of Fe(II) production versus O2 supply, we measured changes in Fe(II) and O2 and in situ •OH production during simulated precipitation events and during common, waterlogged conditions in mesocosms from two landscape ages and the two dominant vegetation types of the Arctic. The balance of Fe(II) production and consumption controlled •OH production during precipitation events that supplied O2 to the soils. During static, waterlogged conditions, •OH production was controlled by O2 supply because Fe(II) production was higher than its consumption (oxidation) by O2. An average precipitation event (4 mm) resulted in 200 µmol •OH m−2 per day produced compared to 60 µmol •OH m−2 per day produced during waterlogged conditions. These findings suggest that the oxidation of DOC to CO2 by •OH in arctic soils, a process potentially as important as microbial respiration of DOC in arctic surface waters, will depend on the patterns and amounts of rainfall that oxygenate the soil.