Functional phases define the response of the soil microbiome to environmental change

A major challenge in microbiome research is understanding how natural communities respond to environmental change. The ecological, spatial, and chemical complexity of soils makes understanding the metabolic response of these communities to perturbations particularly challenging. Here we measure the dynamics of respiratory nitrate utilization in >1,500 soil microcosms from 20 soil samples subjected to pH perturbations. Despite the complexity of the soil microbiome a minimal mathematical model with two parameters, the quantity of active biomass and the availability of a limiting nutrient, quantifies observed nitrate utilization dynamics across soils and pH perturbations. Across environmental perturbations, the model reveals the existence of three functional phases each with distinct qualitative dynamics of nitrate utilization over time: a phase where acidic perturbations induce cell death that limits metabolic activity, a nutrient-limiting phase where nitrate uptake is performed by dominant taxa that utilize nutrients released from the soil matrix, and a resurgent growth phase in basic conditions, where nutrients are in excess and rare taxa rapidly outgrow dominant populations. The underlying mechanism of each phase is predicted by our interpretable model and tested via amendment experiments, nutrient measurements, and sequencing. Finally, our data suggest that how soils transition between functional phases depends on the long-term history of environmental variation in the wild. Therefore, quantitative measurements and a minimal mathematical formalism reveal the existence of qualitative phases that capture the mechanisms and dynamics of a community responding to environmental change.