The microbial control of biogeochemistry in thawing soil

Climate change will lead to warming but also a higher frequency of extreme weather events. These changes will expose frozen soils to more thaw events. Recent work has shown that drying-rewetting (DRW) may trigger two distinct bacterial growth responses depending on the severity of the drought stress. Bacteria either start growing immediately and linearly following rewetting, associated with exponentially decreasing respiration from maximal levels immediately after rewetting (Type 1), or bacterial growth starts increasing exponentially after an extensive lag period (<30h) after rewetting, co-occurring with maintained high levels of respiration during the lag, and a subsequent secondary increase in sync with the growth increase (Type 2). Events of freeze-thaw (FT) present mechanistic similarities to those of DRW since soil water availability is reduced by both drying and freezing, while both rewetting and thawing can reverse the effects. Despite these similarities, it remains unknown if they share a similar microbial regulation. We hypothesized (H1) that type 1 and 2 microbial responses to DRW would also be induced by a FT cycle, but with less pronounced differences than between DRW, due to the smaller water potential reduction by freezing than drying. We also hypothesized (H2) that repeated DRW cycles would accelerate microbial growth recoveries to DRW, but also to FT, and vice versa. We hypothesized (H3) that a higher frequency of FT cycles resulting from warming subarctic soils would give rise to enhanced microbial resilience to FT cycles, and (H4) that thawing permafrost soils would trigger the most extreme type 2 response so far observed. We addressed these hypotheses by (1) comparing microbial responses to DRW and FT in one type 1 soil, and in one type 2 soil. We then (2) exposed the set of two soils to a regime of 1-3 FT or DRW cycles, followed by another characterization of the microbial responses to DRW and FT. Finally, (3) we assessed if exposing a subarctic soil to winter-warming field treatments (+5°C) and increasing the number of FT events affected the microbial responses to a FT cycle, and characterized microbial growth and biogeochemical responses in thawing permafrost compared to samples from the active layer exposed to FT. We found that (H1) microbes recovered growth rates more slowly and respired more in response to DRW than to FT in both type 1 and type 2 soils, and fungal growth was promoted during DRW-induced lag period of bacteria. We also found that (H2) both an increasing number of cycles of FT and DRW could accelerate the bacterial growth recovery to both FT and DRW while fungal growth recovery was unaffected, but that exposure to 1-3 DRW cycles accelerated bacterial growth responses to both FT and DRW more than exposure to 1-3 FT cycles could, in both type 1 and 2 soils. Finally, (H3) winter-warming induced an accelerated bacterial growth recovery, slowed the fungal growth recovery, and enhanced the microbial carbon-use efficiency during the perturbation, while (H4) thawing permafrost resulted in the longest microbial lag periods so far documented.