Prions are a common mechanism for phenotypic inheritance in wild yeasts

• Published in: Nature (London) 2012-02, Vol.482 (7385), p.363-368
• Main Authors: Halfmann, Randal, Jarosz, Daniel F., Jones, Sandra K., Chang, Amelia, Lancaster, Alex K., Lindquist, Susan
• Format: Article
• Language: English
• Subjects: 631/181; 631/208/726/649; 631/45/460; Analytical, structural and metabolic biochemistry; Antibiotics; Biological and medical sciences; Biological Evolution; Cell Wall - metabolism; Cloning; Cytoplasm - metabolism; Epigenesis, Genetic; Fundamental and applied biological sciences. Psychology; Genetic Association Studies; Genetic Variation - genetics; Genetics; Genotype; Heat-Shock Proteins - genetics; Heat-Shock Proteins - metabolism; Humanities and Social Sciences; Laboratories; Meiosis; Microbiology; Molecular and cellular biology; multidisciplinary; Mutation; Non conventional transmissible agents; Peptide Termination Factors - genetics; Peptide Termination Factors - metabolism; Phenotype; Prions; Prions - genetics; Prions - metabolism; Protein folding; Saccharomyces; Saccharomyces cerevisiae - classification; Saccharomyces cerevisiae - cytology; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - metabolism; Saccharomyces cerevisiae Proteins - genetics; Saccharomyces cerevisiae Proteins - metabolism; Science; Science (multidisciplinary); Stress; Transcription Factors - genetics; Transcription Factors - metabolism; Yeasts
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature10875

The self-templating conformations of yeast prion proteins act as epigenetic elements of inheritance. Yeast prions might provide a mechanism for generating heritable phenotypic diversity that promotes survival in fluctuating environments and the evolution of new traits. However, this hypothesis is highly controversial. Prions that create new traits have not been found in wild strains, leading to the perception that they are rare ‘diseases’ of laboratory cultivation. Here we biochemically test approximately 700 wild strains of Saccharomyces for [ PSI + ] or [ MOT3 + ], and find these prions in many. They conferred diverse phenotypes that were frequently beneficial under selective conditions. Simple meiotic re-assortment of the variation harboured within a strain readily fixed one such trait, making it robust and prion-independent. Finally, we genetically screened for unknown prion elements. Fully one-third of wild strains harboured them. These, too, created diverse, often beneficial phenotypes. Thus, prions broadly govern heritable traits in nature, in a manner that could profoundly expand adaptive opportunities. Previously thought to be rare laboratory artefacts or diseases of yeast, prions are actually found in one third of 700 wild strains; the prions give their hosts beneficial traits that can be transmitted epigenetically to the next generation, and then fixed in the genome. Natural prions give yeasts the edge It has been suggested that prions — proteins that undergo transmissible conformation changes — serve as elements of inheritance and evolutionary 'facilitators' in yeast, but many still consider fungal prions to be rare laboratory 'diseases'. Now Susan Lindquist and colleagues have screened 700 yeast strains collected from the wild and found 'natural' prions in one-third of them. They also show that many of these natural prions endow their hosts with traits that are either directly beneficial in specific culture conditions or provide favourable ground for further, DNA-based traits to evolve.