Using tropical heat to investigate adaptive responses of microbial thermal traits and carbon cycling in an in situ translocation experiment

Climate warming can stimulate soil microbial degradation of organic matter, leading to increases in both microbial growth and CO₂ release into the atmosphere. If microbial growth or respiration outpaces the other in response to warming, it can alter the carbon-use efficiency, potentially leading to either increased carbon storage or release. Understanding the temperature-adaptive responses of soil decomposer microbes is thus essential, as they may significantly influence the balance of C between soil and atmosphere. In this study, we used a “space-for-time” substitution to test the impact of environmental temperature change on microbial carbon cycling in soils from a tropical elevation gradient in Chirripó, Costa Rica, using an in situ reciprocal 7-month transplant experiment to low and high elevation. We hypothesized (H1) that the transplantation of samples will shift microbial thermal traits. Specifically, we expected cold transplants to shift the traits of microbes from warm soils toward cool-adapted traits, while warm transplants would shift the traits of microbes from cold soils toward warm-adapted traits. Additionally, warming accelerates microbial use of organic matter (OM), depleting high-quality soil carbon, while cooling slows it, preserving carbon quality. This shift in carbon quality should increase microbial growth in warm soils under cold conditions and decrease growth in cold soils under warm conditions at a standard temperature (H2).  Furthermore, based on the carbon-quality temperature (CQT) hypothesis we expected that the cold transplant will reduce temperature sensitivity (Q₁₀) for microbes from warmer soils, while the warm transplant would increase Q₁₀ for microbes from colder soils (H3).

To estimate microbial thermal traits, microbial growth (bacterial growth and fungal growth) and respiration were estimated at 10 different temperature conditions (0, 5, 10, 15, 20, 25, 30, 35, 40 and 45 °C). We found a significant cool-shift in microbial growth thermal traits after the cold transplant and warm-shifted thermal traits after the warm transplant. These changes led to a marked shift in thermal traits along the elevation gradient, indicating a strong legacy effect of ecosystem differences in temperature and a relatively minor influence of the 7-month transplant experiment. However, the warm transplant had a pronounced influence, driving the microbial growth traits of all samples closer to those of microbes with a warm-ecosystem origin. For respiration thermal traits, the transplant experiment did not alter thermal traits but did affect the respiration rate. The cold transplant reduced microbial respiration in soils with a history of warm temperatures, whereas the warm transplant increased respiration in soils with a history of colder temperatures. We did not find a significant effect of the transplants on bacterial growth and fungal growth rates, but total microbial growth rates tended to increase with MAT.  In support of the CQT hypothesis, we observed a decrease in Q₁₀ for bacterial growth following the cold transplant in soils with a history of warmer temperature, and a strong increase in Q₁₀ for both bacterial growth and respiration.