Elevated mass-specific soil microbial growth rates and no sign of thermal acclimation at a long-term warming gradient

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Warming increases soil microbial respiration which leads to significant soil C loss. However, it has been shown that the initial increase in soil respiration tends to level off in the long term, sometimes even returning to pre-warming levels. Two main hypotheses explain this short-lived thermal respiration increase: (i) The concentration of C substrate in soils declines due to increased microbial activity, becoming a limiting factor and leading to reduced overall respiration, or (ii) Microbial physiology adjusts to higher temperatures to improve fitness under new environmental conditions. The latter concept of a physiological thermal acclimation predicts that microbes in soils exposed to long-term warming will exhibit lower mass-specific growth and respiration rates at a given temperature compared to those at ambient levels. The main objective of this study was to separate the roles of microbial acclimation and substrate limitation in reducing the response of soil respiration to long-term warming. We examined the microbial respiration and growth rates along long-term (>50 years) geothermal warming gradients in Iceland (ForHOT experiment). Soils collected at multiple temperature steps between ambient temperature and +15 °C field warming were incubated in the laboratory at their respective field temperatures. In addition, soils collected from the ambient sites were incubated the same temperatures as the field-warmed soils. Soils were labelled with deuterium-enriched water during incubation, followed by extraction of phospholipid fatty acids (PLFAs). Analyzing the 2H incorporation into PLFAs by Gas Chromatography coupled to isotope ratio mass spectrometry (GC-IRMS) allowed us to estimate group-specific microbial growth rates.When incubated at the same temperatures, soils exposed to long-term warming exhibited lower overall respiration rates (per gram of soil) compared to ambient soils. However, the respiration rate per unit of microbial biomass remained comparable between warmed and ambient. This suggests that the reduction in total respiration is likely due to carbon depletion and a subsequent decrease in overall microbial biomass, rather than a thermal acclimation. Interestingly, at long-term warmed field sites, mass-specific growth rates were considerably higher than those observed in ambient soils subjected to short-term warming at the same temperature. This finding also contradicts the thermal acclimation hypothesis, indicating that prolonged warming does not diminish the temperature response of microbial activity. Instead, our results demonstrate that – on a per unit of microbial biomass basis – long-term microbial temperature response is even more pronounced compared to immediate warming. The disparity between long-term and short-term temperature responses varied among microbial groups. While Firmicutes displayed similar growth responses to warming in both scenarios, fungi and gram-negative bacteria showed significantly higher mass-specific growth rates in long-term warmed plots compared to ambient soils exposed to corresponding levels of short-term warming. These results demonstrate that changes in microbial community function and composition following warming run counter to the typical concept of thermal acclimation.

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