Arctic soil C and N cycling are linked with microbial adaptations during drought

In many regions, climate change increases the frequency and intensity of drought events, yet the mechanisms by which microbial drought responses affect soil carbon (C) and nitrogen (N) cycling are poorly understood, especially for Arctic soils. To study these mechanisms, we conducted a microcosm experiment with a Greenlandic soil subjected to five levels of drought, reducing water content from 180% to 15% over the course of three weeks followed by rewetting, mimicking a natural drought event. We linked changes in microbial gene expression related to stress response as well as C and N cycling with greenhouse gas (GHG) emissions, extracellular enzyme activities and soil C and N status. We revealed maximum changes in gene expression at intermediate levels of drought (80% water content), characterized by acclimation of microbial physiology to drought conditions, including production of osmolytes as well as cell wall and membrane modifications. This peak in gene expression changes marked a tipping point associated with a pronounced decline in microbial respiration as well as extracellular enzyme activities under more intense drought conditions. Interestingly, C-cycling gene expression structures and the expression of specific C-cycling genes correlated with soil dissolved organic nitrogen (DON), NH4+, NO3- and PO43- contents. Moreover, N-cycling gene expression structures and expression of specific N-cycling genes correlated with PO43- contents and with the activity of laccases, key enzymes in lignin degradation. These findings highlight linkages between microbial C, N and P cycling due to stoichiometric constraints under drought. 24 h after rewetting, we found a shift in microbial expression of C usage genes towards more labile compounds, and an increase in genes related to anabolic activity and signalling, but no signatures of stress responses, suggesting that the microbial community had overcome rewetting-induced changes in osmotic pressure and allocated metabolic activity to growth. Overall, we show that microbial physiological drought responses and microbial resource usage related to C:N:P stoichiometry are key mechanisms of C and N cycling in the Arctic soil under drying and rewetting.