Emergence of stable coexistence in a complex microbial community through metabolic cooperation and spatio-temporal niche partitioning

Microbial communities in nature often feature complex compositional dynamics yet also stable coexistence of diverse species. The mechanistic underpinnings of such dynamic stability remain unclear as system-wide studies have been limited to small engineered communities or synthetic assemblies. Here we show how kefir, a natural milk-fermenting community, realizes stable coexistence through spatio-temporal orchestration of species and metabolite dynamics. During milk fermentation, kefir grains (a polysaccharide matrix synthesized by kefir microbes) grow in mass but remain unchanged in composition. In contrast, the milk is colonized in a dynamic fashion with early members opening metabolic niches for the followers. Through large-scale mapping of metabolic preferences and inter-species interactions, we show how microbes poorly suited for milk survive in, and even dominate, the community through metabolic cooperation and uneven partitioning between the grain and the liquid phase. Overall, our findings reveal how spatio-temporal dynamics promote stable coexistence and have implications for deciphering and modulating complex microbial ecosystems.