From dry to thrive: Increased metabolic activity, potassium content and a shift towards fungi after drying-rewetting reveals adjustment of the microbial community to osmotic stress

Abstract

Climate change causes temperature increase and alteration of precipitation patterns with frequent droughts. These are known to influence soil microorganisms leading to community shifts and physiological adaptations, with consequences for biogeochemical cycles. However, whether soil microbial communities evolved at different average temperature differ in their response to drought is not well understood. Therefore, we collected ten soil samples per site (0–30 cm soil depth) from a walnut-fruit forest at 1000, 1300 and 1600 m above sea level with similar vegetation which represent average temperature differences of 1.3 °C between sites, mimicking potential climate change. We incubated these for 70 days at 22 °C either at (i) constant moisture of 50 % soil water holding capacity, or subjected them to (ii) two or (iii) three drying-rewetting (DRW) cycles. Respiration was measured during the incubation; microbial and chemical properties were determined at the end. No elevation specific or interactive effects with DRW were detected, except for fungal gene abundance, where values were highest at the intermediate elevation level. This reveals that soil microbial communities evolved at different average temperature regimes do not differ in their response to drought. Therefore, data were pooled across all sites and analyzed for the main effects of DRW. Microbial activity increased with DRW as reflected by enhanced net‑nitrogen mineralization and basal respiration. However, microbial biomass carbon and ergosterol were reduced by 20 and 25 % and bacterial gene abundance between 20 and 40 %. This reflects the strong osmotic pressure of DRW causing death of microbial cells. The higher maintenance requirements for cell adjustment to osmotic pressure of surviving microorganisms was revealed by an increase of the metabolic quotient qCO₂ by 60 % and accumulation of potassium in the microbial biomass. Fungi cope better with DRW as shown by higher fungal gene abundance as well as their ratio to ergosterol after DRW, reflecting shifts in cell volume due to community shifts or morphological adaptations. Our findings highlight that soil microbial communities evolved under different average temperature regimes respond similarly to DRW, but overall shift towards fungi as this taxon can potentially physiologically better adapt to osmotic pressure. Consequently, DRW may cause higher organic matter turnover and nutrient release due to higher microbial maintenance costs for osmotic cell adjustments.