Microbial responses to soil cooling might explain increases in microbial biomass in winter

In temperate, boreal and arctic soil systems, microbial biomass often increases during winter and decreases again in spring. This build-up and release of microbial carbon could potentially lead to a stabilization of soil carbon during winter times. Whether this increase is caused by changes in microbial physiology, in community composition, or by changed substrate allocation within microbes or communities is unclear. In a laboratory incubation study, we looked into microbial respiration and growth, as well as microbial glucose uptake and carbon resource partitioning in response to cooling. Soils taken from a temperate beech forest and temperate cropland system in October 2020, were cooled down from field temperature of 11 °C to 1 °C. We determined microbial growth using 18O-incorporation into DNA after the first two days of cooling and after an acclimation phase of 9 days; in addition, we traced 13C-labelled glucose into microbial biomass, CO2 respired from the soil, and into microbial phospholipid fatty acids (PLFAs). Our results show that the studied soil microbial communities responded strongly to soil cooling. The 18O data showed that growth and cell division were reduced when soils were cooled from 11 to 1 °C. Total respiration was also reduced but glucose uptake and glucose-derived respiration were unchanged. We found that microbes increased the investment of glucose-derived carbon in unsaturated phospholipid fatty acids at colder temperatures. Since unsaturated fatty acids retain fluidity at lower temperatures compared to saturated fatty acids, this could be interpreted as a precaution to reduced temperatures. Together with the maintained glucose uptake and reduced cell division, our findings show an immediate response of soil microorganisms to soil cooling, potentially to prepare for freezing events. The discrepancy between C uptake and cell division could explain previously observed high microbial biomass carbon in temperate soils in winter.