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Abstract Climate warming has increased permafrost thaw in arctic tundra and extended the duration of annual thaw (number of thaw days in summer) along soil profiles. Predicting the microbial response to permafrost thaw depends largely on knowing how increased thaw duration affects the composition of the soil microbiome. Here, we determined soil microbiome composition from the annually thawed surface active layer down through permafrost from two tundra types at each of three sites on the North Slope of Alaska, USA. Variations in soil microbial taxa were found between sites up to ~90 km apart, between tundra types, and between soil depths. Microbiome differences at a site were greatest across transitions from thawed to permafrost depths. Results from correlation analysis based on multi‐decadal thaw surveys show that differences in thaw duration by depth were significantly, positively correlated with the abundance of dominant taxa in the active layer and negatively correlated with dominant taxa in the permafrost. Microbiome composition within the transition zone was statistically similar to that in the permafrost, indicating that recent decades of intermittent thaw have not yet induced a shift from permafrost to active‐layer microbes. We suggest that thaw duration rather than thaw frequency has a greater impact on the composition of microbial taxa within arctic soils. 

Summary 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 analysed for gene expression and DOM chemical composition. Microbial gene expression (metatranscriptomics) in light and dark treatments diverged substantially after 4 h. Gene expression suggested that sunlight exposure of DOM initially stimulated microbial growth by (i) replacing the function of enzymes that degrade higher molecular weight DOM such as enzymes for aromatic carbon degradation, oxygenation, and decarboxylation, and (ii) 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.