Selection on plastic adherence leads to hyper-multicellular strains and incidental virulence in the budding yeast

Many disease-causing microbes are not obligate pathogens; rather, they are environmental microbes taking advantage of an ecological opportunity. The existence of microbes that are not normally pathogenic, yet are well-suited to host exploitation, is an evolutionary paradox. One hypothesis posits that selection in the environment may favor traits that incidentally lead to pathogenicity and virulence, or serve as pre-adaptations for survival in a host. An example of such a trait is surface adherence. To experimentally test the idea of “accidental virulence”, replicate populations of the yeast, Saccharomyces cerevisiae, which can be an opportunistic pathogen, were evolved to attach to a plastic bead for hundreds of generations. Along with plastic adherence, two multicellular phenotypes— biofilm formation and flor formation— increased; another phenotype, pseudohyphal growth, responded to the nutrient limitation. Thus, experimental selection led to the evolution of highly-adherent, hyper-multicellular strains. Wax moth larvae injected with evolved hyper-multicellular strains were significantly more likely to die than those injected with evolved non-multicellular strains. Hence, selection on plastic adherence incidentally led to the evolution of enhanced multicellularity and increased virulence. Our results support the idea that selection in the environment for a trait unrelated to virulence can inadvertently generate opportunistic, “accidental” pathogens.