The natural history of yeast prions

Although prions were first discovered through their link to severe brain degenerative diseases in animals, the emergence of prions as regulators of the phenotype of the yeast Saccharomyces cerevisiae and the filamentous fungus Podospora anserina has revealed a new facet of prion biology. In most cases, fungal prions are carried without apparent detriment to the host cell, representing a novel form of epigenetic inheritance. This raises the question of whether or not yeast prions are beneficial survival factors or actually gives rise to a "disease state" that is selected against in nature. To date, most studies on the impact of fungal prions have focused on laboratory-cultivated "domesticated" strains of S. cerevisiae. At least eight prions have now been described in this species, each with the potential to impact on a wide range of cellular processes. The discovery of prions in nondomesticated strains of S. cerevisiae and P. anserina has confirmed that prions are not simply an artifact of "domestication" of this species. In this review, I describe what we currently know about the phenotypic impact of fungal prions. I then describe how the interplay between host genotype and the prion-mediated changes can generate a wide array of phenotypic diversity. How such prion-generated diversity may be of benefit to the host in survival in a fluctuating, often hazardous environment is then outlined. Prion research has now entered a new phase in which we must now consider their biological function and evolutionary significance in the natural world.