Stress-induced cross-feeding of internal metabolites provides a dynamic mechanism of microbial cooperation

Metabolic cross-feeding plays vital roles in promoting ecological diversity. While some microbes depend on exchanges of essential nutrients for growth, forces driving the extensive cross-feeding needed to support the coexistence of free-living microbes are poorly understood. Here we characterize bacterial physiology under self-acidification, and establish that extensive excretion of key metabolites following acidification provides a collaborative, inter-species mechanism of stress resistance. This collaboration occurs not only between species isolated from the same community, but also between unrelated species with complementary (glycolytic vs. gluconeogenic) modes of metabolism. Cultures of such communities cycle through different phases in growth-dilution experiments, comprising of exponential growth, growth arrest upon acidification, collaborative stress relief, and growth recovery, with each phase involving distinct physiological states of individual species. Our findings challenge the static view of ecosystems commonly portrayed in ecological models, and offer an alternative dynamical view based on growth advantages of different species in different phases.