Stronger compensatory thermal adaptation of soil microbial respiration with higher substrate availability

Abstract

Ongoing global warming is expected to augment soil respiration by increasing the microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and we incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modeled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, which is consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when the substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences the soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.

Keywords: global warming; microbial respiration; microbial thermal adaptation; soil carbon decomposition.

Figure 1

Conceptual paradigm depicting the effect of substrate availability on microbial thermal adaptation; (a) compensatory thermal adaptation of microbial respiration rate to climate warming, that is respiration rate at the mean microbial biomass across all sites decreases with increasing MAT; we hypothesized that microbial respiration rate was higher in soils from colder environments than those from warmer environments when incubated at the same incubation temperature (T); further, the differences in respiration rates between incubation temperatures should be larger for samples from colder environments than for those from warmer environments because thermal adaptation effects should be greater in warmer regions; (b) microbial respiration rate increases with increasing MAT during incubation at T = MAT under excess substrate addition (A₁ and A₂) and substrate depletion (B₁ and B₂); microbial respiration rate is higher when substrate is added than without it (e.g. B₁ < A₁ or B₂ < A₂) due to substrate depletion effect; thus, the substrate depletion effect without thermal adaptation is calculated as A₁ − B₁ at the same T; accordingly, the substrate depletion effect with thermal adaptation is calculated as A₂ − B₂; microbial respiration rate is lower with microbial thermal adaptation than without adaptation due to the compensatory response (e.g. A₂ < A₁ or B₂ < B₁); thus, the microbial thermal adaptation effect with substrate addition is calculated as A₁ − A₂ at the same T; accordingly, the microbial thermal adaptation effect with substrate depletion is calculated as B₁ − B₂; the overall difference in microbial respiration A₁ − B₂ is because of either the microbial thermal adaptation and the interaction of microbial thermal adaptation with substrate depletion, or substrate depletion and interaction of substrate depletion with microbial thermal adaptation.

Figure 2

Model estimated effects of MAT on microbial respiration without and with substrate addition; (a) and (b) for the dataset from this study; (c) and (d) for the dataset from Bradford et al. [18]; (e) and (f) for the dataset from Dacal et al. [31]; microbial respiration rates (points) were estimated using the unstandardized coefficients from models given in Table 1, by increasing MAT and incubation temperature values in the regression equation systematically from the lowest to highest values observed in each study, and the values of the other variables (microbial biomass and soil texture) were held as the averages across all sites; the shaded areas show the standard deviation of potential soil microbial respiration rates at each incubation temperature (T).

Figure 3

Estimated effects of microbial thermal adaptation and substrate availability on microbial respiration; (a) for the dataset from this study; (b) for the dataset from Bradford et al. [18]; (c) for the dataset from Dacal et al. [31]; microbial respiration rates (points) were calculated using the unstandardized coefficients from models given in Table 1; for the scenario with thermal adaptation, incubation temperature (T) was set to be the same as MAT, while the other variables (microbial biomass and soil texture) were held at the averages across all sites; by contrast, in the scenario without thermal adaptation, the coefficient of MAT was set to zero; the calculation was conducted for soil incubation with and without substrate addition.

Figure 4

Relative magnitude of microbial thermal adaptation and substrate depletion on microbial respiration; (a) for the dataset from this study; (b) for the dataset from Bradford et al. [18]; (c) for the dataset from Dacal et al. [31]; the point values were calculated using data from Fig. 3 and Equations (12)–(15) given in the Materials and methods; higher values indicate the stronger influence on the overall compensatory response of microbial respiration.