Yeast Creates a Niche for Symbiotic Lactic Acid Bacteria through Nitrogen Overflow

Many microorganisms live in communities and depend on metabolites secreted by fellow community members for survival. Yet our knowledge of interspecies metabolic dependencies is limited to few communities with small number of exchanged metabolites, and even less is known about cellular regulation facilitating metabolic exchange. Here we show how yeast enables growth of lactic acid bacteria through endogenous, multi-component, cross-feeding in a readily established community. In nitrogen-rich environments, Saccharomyces cerevisiae adjusts its metabolism by secreting a pool of metabolites, especially amino acids, and thereby enables survival of Lactobacillus plantarum and Lactococcus lactis. Quantity of the available nitrogen sources and the status of nitrogen catabolite repression pathways jointly modulate this niche creation. We demonstrate how nitrogen overflow by yeast benefits L. plantarum in grape juice, and contributes to emergence of mutualism with L. lactis in a medium with lactose. Our results illustrate how metabolic decisions of an individual species can benefit others. [Display omitted] •Yeast overflows amino acids that enable survival of lactic acid bacteria (LAB)•Overflow is in proportion to nitrogen excess and regulated via TORC1 pathway•Phenotype supporting LAB growth is conserved across diverse yeast isolates•Yeast-LAB mutualism readily emerges when lactose is the main C-source Yeast and LAB co-occur in a variety of naturally fermented foods and beverages. We show, using metabolomics, transcriptomics, and genetic analysis, how nitrogen overflow by yeast benefits LAB and contributes to the emergence of mutualism.