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The metabolic activity of microbial communities is essential for host and environmental health, influencing processes from immune regulation to bioremediation. Given this importance, the rational design of microbiomes with targeted functional properties is an important objective. Designing microbial consortia with targeted functions is challenging due to complex community interactions and environmental heterogeneity. Community-function landscapes address this challenge by statistically inferring impacts of species presence or absence on function. Similar to fitness landscapes, community-function landscapes are shaped by both additive effects and interactions (epistasis) among species that influence function. Here, we apply the community-function landscape approach to design synthetic microbial consortia to degrade the toxic environmental contaminant bisphenol-A (BPA). Using synthetic communities of BPA-degrading isolates, we map community-function landscapes across increasing BPA concentrations, where higher BPA means greater toxicity. As toxicity increases, so does epistasis, indicating that collective effects become more important in degradation. Further, we leverage landscapes to rationally design communities with predictable BPA degradation dynamics in vitro. Remarkably, designed synthetic communities are able to remediate BPA in contaminated soils. Our results demonstrate that toxicity can drive epistatic interactions in community-function landscapes and that these landscapes can guide microbial consortia design for bioremediation. 

Abstract The metabolic activity of soil microbiomes plays a central role in carbon and nitrogen cycling. Given the changing climate, it is important to understand how the metabolism of natural communities responds to environmental change. However, the ecological, spatial, and chemical complexity of soils makes understanding the mechanisms governing the response of these communities to perturbations challenging. Here, we overcome this complexity by using dynamic measurements of metabolism in microcosms and modeling to reveal regimes where a few key mechanisms govern the response of soils to environmental change. We sample soils along a natural pH gradient, construct >1500 microcosms to perturb the pH, and quantify the dynamics of respiratory nitrate utilization, a key process in the nitrogen cycle. Despite the complexity of the soil microbiome, a minimal mathematical model with two variables, the quantity of active biomass in the community and the availability of a growth-limiting nutrient, quantifies observed nitrate utilization dynamics across soils and pH perturbations. Across environmental perturbations, changes in these two variables give rise to three functional regimes each with qualitatively distinct dynamics of nitrate utilization over time: a regime where acidic perturbations induce cell death that limits metabolic activity, a nutrientlimiting regime where nitrate uptake is performed by dominant taxa that utilize nutrients released from the soil matrix, and a resurgent growth regime in basic conditions, where excess nutrients enable growth of initially rare taxa. The underlying mechanism of each regime is predicted by our interpretable model and tested via amendment experiments, nutrient measurements, and sequencing. Further, our data suggest that the long-term history of environmental variation in the wild influences the transitions between functional regimes. Therefore, quantitative measurements and a mathematical model reveal the existence of qualitative regimes that capture the mechanisms and dynamics of a community responding to environmental change.