Strong Ethanol- and Frequency-Dependent Ecological Interactions in a Community of Wine-Fermenting Yeasts

Abstract

Natural wine fermentation is carried out by the complex consortia of microorganisms native to grapes and winery equipment, rather than by inoculation with industrial yeast strains. While this diversity of yeasts can result in an increased repertoire of wine flavors and aromas, it can also result in the inhibition of Saccharomyces cerevisiae, which is uniquely able to withstand the high ethanol and low resource conditions in the end stages of fermentation. Understanding how yeast species interact with each other within the wine-fermenting community, and disentangling the importance of these ecological interactions from the environmental impacts on growth rates, is key to developing synthetic communities that can provide the sensory benefits of natural fermentation while lowering the risk of stuck ferments. While numerous studies have characterized the dynamics of experimental fermentations, carried out by both synthetic and natural communities, it is difficult to infer ecological interactions from transient population dynamics. Here, we co-culture all pairwise combinations of five commonly isolated wine-fermenting yeasts at various ethanol concentrations. We show that these pairwise outcomes are a strong function of ethanol concentration, with frequency-dependent bistable interactions common at low alcohol and an increasingly transitive competitive hierarchy developing as alcohol increases. We also show that these pairwise outcomes are predictive of five-species community outcomes, and that frequency dependence in pairwise interactions can propagate to alternative states in the full community, highlighting the importance of species abundance as well as composition. We also observe that monoculture growth rates as a function of ethanol are only weakly predictive of competitive success, highlighting the need to incorporate ecological interactions when designing synthetic communities for optimal fermentation performance.