There are more evidence from soil science that microbial decomposition plays a determinant role in global soil carbon cycling, reflected by the emergence of carbon models representing processes such as soil respiration and soil formation stemming out from microbial decomposition of soil organic matter. Microbial response to warming will therefore strongly influence the direction and amplitude of soil carbon-climate feedbacks. While attention is focused on microbial change in community composition or on individual physiological response, no study has addressed the effect of microbial evolutionary response on the response of soil decomposition to warming. We first built a spatially explicit eco-evolutionary stochastic model of soil decomposition to investigate the microscopic processes of microbial competition over resources and of enzyme-substrate interactions to improve parameterization. We then used the corresponding deterministic eco-evolutionary microbial model of decomposition and tested three scenarios of temperature sensitivity to investigate (i) the evolutionary dynamics of one microbial trait, investment in enzyme production, (ii) how this evolutionary response feeds back on soil carbon stocks, and (iii) where to expect the strongest evolutionary effects at the global scale for which we integrated global projected data of surface soil temperature and litter flux and measured site-specific enzyme traits.
Results/Conclusions
Spatial simulations showed a critical effect of the spatial distribution of individual microbes and of resource diffusivity on competition and therefore on the selected investment in enzyme production. Selected enzyme production was also predicted to be the highest in systems with long-lived organisms that assimilate and use resources efficiently. Microbes evolved a high enough enzyme production to sustain their growth in low diffusive soils. In those conditions, microbes generally adapted to warming by investing more in enzyme production. As a consequence, microbial adaptive evolution was predicted to accelerate decomposition and therefore to increase soil carbon loss predicted by purely ecological models. All scenarios of temperature sensitivity predicted the strongest carbon loss and evolutionary effects in cold ecosystems. The one scenario of temperature sensitivity tested at the global scale predicted a 33% global aggravation of carbon loss due to microbial evolution with higher contributions from regions at higher latitudes. Our results highlight the pressing need to investigate experimentally microbial evolutionary response to climate change and to include soil eco-evolutionary feedbacks to carbon cycling in global climate models.