From Metabolism to Ecology: Cross-Feeding Interactions Shape the Balance between Polymicrobial Conflict and Mutualism

Polymicrobial interactions are widespread in nature and play a major role in maintaining human health and ecosystems. Whenever one organism uses metabolites produced by another organism as energy or nutrient sources, it is called cross-feeding. The ecological outcomes of cross-feeding interactions are poorly understood and potentially diverse: mutualism, competition, exploitation, or commensalism. A major reason for this uncertainty is the lack of theoretical approaches linking microbial metabolism to microbial ecology. To address this issue, we explore the dynamics of a one-way interspecific cross-feeding interaction in which food can be traded for a service (detoxification). Our results show that diverse ecological interactions (competition, mutualism, exploitation) can emerge from this simple cross-feeding interaction and can be predicted by the metabolic, demographic, and environmental parameters that govern the balance of the costs and benefits of association. In particular, our model predicts stronger mutualism for intermediate by-product toxicity because the resource-service exchange is constrained to the service being neither too vital (high toxicity impairs resource provision) nor dispensable (low toxicity reduces need for service). These results support the idea that bridging microbial ecology and metabolism is a critical step toward a better understanding of the factors governing the emergence and dynamics of polymicrobial interactions.