Many disease-causing microbes are not obligate pathogens; rather, they are environmental microbes taking advantage of an ecological opportunity. The existence of microbes whose life cycle does not require a host and are not normally pathogenic, yet are well-suited to host exploitation, is an evolutionary puzzle. 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 Saccharomyces cerevisiae 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 for a trait beneficial in the open environment can inadvertently generate opportunistic, 'accidental' pathogens.
Keywords: FLO11; S. cerevisiae; adherence; biofilm; evolutionary biology; experimental evolution; infectious disease; microbiology; virulence; wax moth; yeast.
Yeast are microscopic fungi that are found on many plants, in the soil and in other environments around the world. But, when given the chance, some yeasts are also good at infecting human and other animals and causing disease. It has been proposed that some opportunistic microbes may have dual-use traits that evolved for one purpose in their natural environment but also incidentally allow them to infect animals. For example, a toxin that helps the opportunistic microbe compete against neighboring microbes may also weaken an animal. Or the ability of many individual microbe cells to clump together into structures known as biofilms on solid surfaces, or floating mats called flors on liquids, helps them to survive in harsh environments, whether in the soil or in the body of an animal. To investigate this possibility, Ekdahl, Salcedo et al. examined whether artificially selecting yeast with a specific trait – the ability to stick to plastic beads – in the absence of any host animals would inadvertently also select for yeast that were good at causing disease. This trait was selected because it has not been previously linked to opportunistic yeast infections. The team grew the yeast for 400 generations in tubes that each contained a plastic bead. At every generation, only yeast that stuck to the plastic bead were transferred to a fresh tube to grow the next generation. The experiments found that, not only did the ability of the yeast to stick to the plastic increase over time, but the yeast also evolved the ability to form biofilms and flors. Furthermore, the sticky yeast killed an insect host known as wax moth larvae more quickly than non-sticky yeast. Together, these findings demonstrate that when microbes evolve in an environment that is devoid of any host animals, selection can inadvertently favor dual-use traits that also help the yeast to infect animals. Opportunistic yeast infections are of increasing concern in human patients, particularly those with weakened immune systems. Understanding which yeast traits are dual-use will help guide future efforts in combatting yeast and other opportunistic microbes.
© 2023, Ekdahl, Salcedo et al.