Rainfall Alters Permafrost Soil Redox Conditions, but Meta-Omics Show Divergent Microbial Community Responses by Tundra Type in the Arctic

Abstract

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.