Subarctic winter warming promotes soil microbial resilience to freeze-thaw cycles and enhances the microbial carbon use efficiency.

Climate change is predicted to cause milder winters and thus exacerbate soil freeze-thaw perturbations in the subarctic, recasting the environmental challenges that soil microorganisms need to endure. Historical exposure to environmental stressors can facilitate the microbial resilience to new cycles of that same stress. However, whether and how such microbial memory or stress legacy can modulate microbial responses to cycles of frost remains untested. Here, we conducted an in situ field experiment in a subarctic birch forest, where winter warming resulted in a substantial increase in the number and intensity of freeze-thaw events. After one season of winter warming, which raised mean surface and soil (-8 cm) temperatures by 2.9 and 1.4°C, respectively, we investigated whether the in situ warming-induced increase in frost cycles improved soil microbial resilience to an experimental freeze-thaw perturbation. We found that the resilience of microbial growth was enhanced in the winter warmed soil, which was associated with community differences across treatments. We also found that winter warming enhanced the resilience of bacteria more than fungi. In contrast, the respiration response to freeze-thaw was not affected by a legacy of winter warming. This translated into an enhanced microbial carbon-use efficiency in the winter warming treatments, which could promote the stabilization of soil carbon during such perturbations. Together, these findings highlight the importance of climate history in shaping current and future dynamics of soil microbial functioning to perturbations associated with climate change, with important implications for understanding the potential consequences on microbial-mediated biogeochemical cycles.

Heat wave-induced microbial thermal trait adaptation and its reversal in the Subarctic.

Climate change predictions suggest that arctic and subarctic ecosystems will be particularly affected by rising temperatures and extreme weather events, including severe heat waves. Temperature is one of the most important environmental factors controlling and regulating microbial decomposition in soils; therefore, it is critical to understand its impact on soil microorganisms and their feedback to climate warming. We conducted a warming experiment in a subarctic birch forest in North Sweden to test the effects of summer heat waves on the thermal trait distributions that define the temperature dependences for microbial growth and respiration. We also determined the microbial temperature dependences 10 and 12 months after the heat wave simulation had ended to investigate the persistence of the thermal trait shifts. As a result of warming, the bacterial growth temperature dependence shifted to become warm-adapted, with a similar trend for fungal growth. For respiration, there was no shift in the temperature dependence. The shifts in thermal traits were not accompanied by changes in α- or ß-diversity of the microbial community. Warming increased the fungal-to-bacterial growth ratio by 33% and decreased the microbial carbon use efficiency by 35%, and both these effects were caused by the reduction in moisture the warming treatments caused, while there was no evidence that substrate depletion had altered microbial processes. The warm-shifted bacterial thermal traits were partially restored within one winter but only fully recovered to match ambient conditions after 1 year. To conclude, a summer heat wave in the Subarctic resulted in (i) shifts in microbial thermal trait distributions; (ii) lower microbial process rates caused by decreased moisture, not substrate depletion; and (iii) no detectable link between the microbial thermal trait shifts and community composition changes.

Variation in Temperature Dependences across Europe Reveals the Climate Sensitivity of Soil Microbial Decomposers.

Temperature is a major determinant of biological process rates, and microorganisms are key regulators of ecosystem carbon (C) dynamics. Temperature controls microbial rates of decomposition, and thus warming can stimulate C loss, creating positive feedback to climate change. If trait distributions that define temperature relationships of microbial communities can adapt to altered temperatures, they could modulate the strength of this feedback, but if this occurs remains unclear. In this study, we sampled soils from a latitudinal climate gradient across Europe. We established the temperature relationships of microbial growth and respiration rates and used these to investigate if and with what strength the community trait distributions for temperature were adapted to their local environment. Additionally, we sequenced bacterial and fungal amplicons to link the variance in community composition to changes in temperature traits. We found that microbial temperature trait distributions varied systematically with climate, suggesting that an increase in mean annual temperature (MAT) of 1°C will result in warm-shifted microbial temperature trait distributions equivalent to an increase in temperature minimum (Tmin) of 0.20°C for bacterial growth, 0.07°C for fungal growth, and 0.10°C for respiration. The temperature traits for bacterial growth were thus more responsive to warming than those for respiration and fungal growth. The microbial community composition also varied with temperature, enabling the interlinkage of taxonomic information with microbial temperature traits. Our work shows that the adaptation of microbial temperature trait distributions to a warming climate will affect the C-climate feedback, emphasizing the need to represent this to capture the microbial feedback to climate change. IMPORTANCE One of the largest uncertainties of global warming is if the microbial decomposer feedback will strengthen or weaken soil C-climate feedback. Despite decades of research effort, the strength of this feedback to warming remains unknown. We here present evidence that microbial temperature relationships vary systematically with environmental temperatures along a climate gradient and use this information to forecast how microbial temperature traits will create feedback between the soil C cycle and climate warming. We show that the current use of a universal temperature sensitivity is insufficient to represent the microbial feedback to climate change and provide new estimates to replace this flawed assumption in Earth system models. We also demonstrate that temperature relationships for rates of microbial growth and respiration are differentially affected by warming, with stronger responses to warming for microbial growth (soil C formation) than for respiration (C loss from soil to atmosphere), which will affect the atmosphere-land C balance.