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

Bernadette M Deschaine,Angela R Heysel,B Adam Lenhart,Helen A Murphy

doi:10.1002/ece3.4082

Abstract

Microbes can engage in social interactions ranging from cooperation to warfare. Biofilms are structured, cooperative microbial communities. Like all cooperative communities, they are susceptible to invasion by selfish individuals who benefit without contributing. However, biofilms are pervasive and ancient, representing the first fossilized life. One hypothesis for the stability of biofilms is spatial structure: Segregated patches of related cooperative cells are able to outcompete unrelated cells. These dynamics have been explored computationally and in bacteria; however, their relevance to eukaryotic microbes remains an open question. The complexity of eukaryotic cell signaling and communication suggests the possibility of different social dynamics. Using the tractable model yeast, Saccharomyces cerevisiae, which can form biofilms, we investigate the interactions of environmental isolates with different social phenotypes. We find that biofilm strains spatially exclude nonbiofilm strains and that biofilm spatial structure confers a consistent and robust fitness advantage in direct competition. Furthermore, biofilms may protect against killer toxin, a warfare phenotype. During biofilm formation, cells are susceptible to toxin from nearby competitors; however, increased spatial use may provide 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 more complex eukaryotes.

Highlights

Social interactions between microbes, both within and between species, are abundant and extremely important
This study investigated the fitness effects of biofilm formation in environmental isolates of the model organism, Saccharomyces cerevisiae; our results suggest a robust advantage in direct competition with nonbiofilm formers in spatially structured communities
Our results support the findings of bacterial and computational studies that show a competitive advantage associated with adhesion and spatial structure (Garcia et al, 2015; Irie et al, 2017; Kim et al, 2014; Schluter et al, 2015; Xavier & Foster, 2007)

Summary

| INTRODUCTION

Both within and between species, are abundant and extremely important. We sought to test the generality of the predictions of microbial social evolution theory for spatially structured communities that have been demonstrated in silico and in bacteria: that biofilm formation provides a strong fitness benefit and that biofilms are a competitive strategy used to obtain resources and exclude other strains (Garcia et al, 2015; Kim et al, 2014; Schluter et al, 2015; Xavier & Foster, 2007) If these results hold true in more complex eukaryotes, they may represent universal principles underlying the stability of biofilms. Toxin production was effective against biofilm-forming strains, we speculate that spatial use may provide a way to escape from toxin-producing competitors

| MATERIALS AND METHODS

Findings

| DISCUSSION