Microbial response to rainfall-altered redox conditions in permafrost soils differs by tundra type

Karl J. Romanowicz and George W. Kling, Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, Byron C. Crump, College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR

Background/Question/Methods
Permafrost soils consist of permanently frozen ground overlain by a shallow, seasonally-thawed active soil layer (the ‘active layer’). Soil anoxia is common in the active layer, particularly when soils are saturated with water, 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. What is unknown is the impact of rainfall and altered redox conditions on the microbial communities, specifically their metabolic capacity for anaerobic CH4 production and aerobic respiration following soil oxidation. To test the impacts of rainfall-induced soil oxidation on microbial communities, we simulated a rainfall event in soil mesocosms from two dominant tundra types, tussock tundra and wet sedge tundra. Our results provide mechanistic explanations for the microbial response to rainfall using an integrated meta-omics approach coupled with soil oxygen modeling. We also conducted a separate soil incubation experiment to measure rates of microbial respiration and CH4 production under anoxic and oxic conditions that mimic pre- and post-rainfall soil redox conditions.
Results/Conclusions
We found that rainfall increased the total soil O2 concentration in both tundra types, 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. As such, our 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, including ribosome transcription, RNA polymerase, and DNA repair. 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 microbial gene expression for aerobic respiration in tussock tundra communities, but may not accumulate or remain in wet sedge tundra soils long enough to induce a community-wide shift away 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.