Abstract
SummaryMany 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.
Highlights
One of the most impactful ecological roles of interspecies metabolite exchange is nutrient cross-feeding
In methanogenic anaerobic consortia methane producers rely on electron carriers supplied by primary fermenters (Embree et al, 2015; Morris et al, 2013; Stams, 1994; Tveit et al, 2015); human gut symbionts degrade complex dietary polysaccharides sequentially, by sharing intermediate metabolites with other community members (Koropatkin et al, 2012; Rakoff-Nahoum et al, 2014; Rios-Covian et al, 2015); and soil bacteria secrete diverse array of metabolites that are available for the other community members (Baran et al, 2015)
A medium for detecting growth-promoting metabolite exchange should strike a balance between scarcity and richness: it should lack components that could be exchanged between community members, and be sufficiently rich to support the growth of all three species
Summary
One of the most impactful ecological roles of interspecies metabolite exchange is nutrient cross-feeding. To circumvent challenges of detecting metabolite exchange in complex natural environments, details of metabolic interactions are usually scrutinized in synthetic communities. These are often constructed using known, evolved, or genetically engineered metabolic interactions (Andrade-Dominguez et al, 2014; Hom and Murray, 2014; Kosina et al, 2016; Mee et al, 2014; Miller et al, 2010; Wintermute and Silver, 2010; Zhou et al, 2015), and have provided insights into principles and mechanics of interspecies dependencies (De Roy et al, 2014; Ponomarova and Patil, 2015; Song et al, 2014). Little is known about the regulatory decisions that prompt a microorganism to secrete valuable metabolites that form the basis of interspecies metabolite exchange
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