Biofilm formation and toxin production provide a fitness advantage in mixed colonies of natural yeast isolates

Abstract

Microbes exist in complex communities and can engage in social interactions ranging from cooperation to warfare. Biofilms are structured, cooperative microbial communities; they are pervasive and ancient, representing the first fossilized life. Like all cooperative communities, biofilms are susceptible to invasion by selfish individuals who benefit from cooperation, but do not contribute. The ubiquity of biofilms therefore poses a challenge to evolutionary theory. One hypothesis for biofilm stability is spatial structure: patches of related cooperative cells are able to outcompete unrelated cells. These dynamics have been explored computationally and in bacterial systems; however, their relevance to eukaryotic microbes remains an open question. Here, we investigate the interactions of environmental yeast isolates with different social phenotypes. Our results show that biofilm strains spatially exclude non-biofilm strains, and that biofilm spatial structure confers a consistent and robust fitness advantage in direct competition. We also find that biofilms protect against killer toxin, a warfare phenotype. During biofilm formation, cells are susceptible to toxin from nearby competitors; however, increased spatial use by biofilms provides an escape from toxin-producers. Our results suggest that yeast biofilms represent a competitive strategy, and that principles elucidated for the evolution and stability of bacterial biofilms may apply to eukaryotes.