Unravelling the processes that govern the emission/sequestration of carbon in soils subjected to moisture changes

Soil moisture is one of the most important variables controlling the activity and diversity of resident microorganisms and play a mediating role in biogeochemical cycling and soil functioning. Yet, natural ecosystems are not exposed to constant moisture conditions but to successive drying and rewetting (D/RW) cycles where periods of drought are interspersed with sudden rainfall events. Soil scientists have known for more than 60 years about the existence of the Birch effect, that is, that the rewetting of a dry soil causes a profound remobilization of resources and a large emission of CO₂ to the atmosphere. However, recent empirical evidence at high temporal resolution has demonstrated that respiration and microbial growth follow strongly disconnected patterns. Moreover, these microbial patterns can be categorized into two general responses: the microbial community starts synthesizing new biomass immediately after rewetting (“type-1”), or after a lag period of several hours (“type-2”). Despite the enormous implications of these short-term dynamics for the stabilization of C in soils and the C budget, they have been surprisingly ignored in biogeochemical models at all scales.

To address this critical issue, we developed a new process-based model (EcoSMMARTS) that incorporated a long list of soil and microbial mechanisms thought to affect the responses to D/RW, based on previous literature. The model was proven useful to reproduce the disconnected behaviour between microbial growth and respiration, and captured the patterns characterizing both types of response. We identified the physiological and structural characteristics of the community at the moment of rewetting as the main factor controlling the patterns of the response. And these characteristics were, in turn, determined by the history of climate, which defined the stress-level of cells and selected for microbial groups with the most suitable survival strategies. The communities better adapted to dry environments could start growing immediately after rewetting and depicted a resilient or “type-1” response, where the elimination of osmolytes to adapt the internal osmotic pressure of cells played a major role. In contrast, those communities from continuously moist environments could not withstand the harshness of the D/RW event and depicted a sensitive response or “type-2”. The small population surviving (and still active) after the drying phase caused a delay in the synthesis of biomass, while cell residues from dead organisms contributed largely to respiration. The C fuelling the emissions was sourced from the accumulation of dead microbial biomass during droughts, and from multiple sources after rewetting, including microbial foraging, the disruption of soil aggregates, and the reuse of osmolytes. The good qualitative agreement between the model results and empirical observations represents a critical step towards unravelling the drivers and key mechanisms that govern the functioning of soils and their feedbacks on climate.