Scaling the impact of microbial ecophysiology on ecosystem-level decomposition rates under drought

Quantifying the influence of drought on microbial processes in soil and its consequences for carbon cycling is hindered by the lack of underlying mechanistic understanding. Drought affects soil microbes directly by causing physiological stress but also affects indirectly by influencing substrate transport and diffusion. Another indirect effect is through changes in plant litter chemistry which impacts microbial resource acquisition strategies. Here we present a theoretical framework to study the effects of drought as well as the ecosystem feedbacks that are generated due to the complex interactions of above-ground and below-ground processes. We classify microbial life history strategies into high yield (Y), resource acquisition (A) and stress tolerance (S), or Y-A-S along two main axes of environmental variation: resources and abiotic stress. We propose the use of this framework that incorporates trait-based ecology to link drought-impacted microbial processes to rates of soil carbon decomposition and stabilisation. We also present empirical evidence in plant litter microbial communities from a decade-long precipitation manipulation experiment in the field in Mediterranean grass and shrub ecosystems in Southern California. Using metagenome-assembled genomes (MAGs), we demonstrate trade-offs in stress tolerance and resource acquisition traits in bacterial populations in grass litter which arise due to selection of certain taxa by drought as the environmental filter. Through taxonomic and MAGs analyses across four time points over 18 months, we observed the dominance of fungi at the start of the litter decomposition process. These fungal pioneers by secreting extracellular enzymes likely enable the survival of drought tolerating bacteria with reduced decomposition capabilities. The indirect effect of drought on plant litter chemistry was examined by FTIR analysis of litter linked to microbial Carbohydrate-Active Enzyme (CAZyme) gene abundance for different substrates which shows subtle shifts in plant litter chemistry and associated changes in microbial resource acquisition traits that were linked to community succession during the decomposition process. We also observed signatures of recycling of fungal and bacterial necromass. Litter decomposition rates measured as mass loss using litter bags were unaffected by drought in shrub ecosystems but showed trends of reduction in grass ecosystems. The integrated knowledge from these studies demonstrates the various mechanisms by which microbial ecophysiology influences decomposition rates under drought and highlights the need for such scaling up of microbial response to climate change factors from individual soil microbes to collective communities to ecosystems.