A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils

•Limited soil water reduces substrate supply to microbes and requires osmoregulation.•We propose a model describing these effects to predict microbial response to drought.•The model allows defining a set of water stress response strategies.•Drought avoiders turn dormant in dry conditions, rather than invest C in osmolytes.•Drought tolerant microbes invest C in osmolytes, but can be active longer.

Soil microbes face highly variable moisture conditions that force them to develop adaptations to tolerate or avoid drought. Drought conditions also limit the supply of vital substrates by inhibiting diffusion in dry conditions. How these biological and physical factors affect carbon (C) cycling in soils is addressed here by means of a novel process-based model. The model accounts for different microbial response strategies, including different modes of osmoregulation, drought avoidance through dormancy, and extra-cellular enzyme production. Diffusion limitations induced by low moisture levels for both extra-cellular enzymes and solutes are also described and coupled to the biological responses. Alternative microbial life-history strategies, each encoded in a set of model parameters, are considered and their effects on C cycling assessed both in the long term (steady state analysis) and in the short term (transient analysis during soil drying and rewetting). Drought resistance achieved by active osmoregulation requiring large C investment is not useful in soils where growth in dry conditions is limited by C supply. In contrast, dormancy followed by rapid reactivation upon rewetting seems to be a better strategy in such conditions. Synthesizing more enzymes may also be advantageous because it causes larger accumulation of depolymerized products during dry periods that can be used upon rewetting. Based on key model parameters, a spectrum of life-history strategies thus emerges, providing a possible classification of microbial responses to drought.

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