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

Abstract

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 how these communities respond metabolically 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. The model reveals three distinct functional phases that encode the low-dimensional dynamics of nitrate utilization in response to short and long-term pH perturbations: a phase where acidic perturbations induce cell death that limits metabolic activity, a nutrient-limiting phase where nitrate utilization 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 functional mechanism of each phase is revealed by our interpretable model and tested via amendment experiments, nutrient measurements, and sequencing. The long-term pH of the soil determines the size of pH changes necessary to drive transitions between functional phases. Our results unify decades of previous studies on nitrogen utilization and pH in soils under a single quantitative framework. A minimal mathematical formalism reveals the existence of a few qualitative phases that capture the mechanisms and dynamics of a community responding to environmental change.