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SummaryPrion proteins undergo self-sustaining conformational conversions that heritably alter their activities. Many of these proteins operate at pivotal positions in determining how genotype is translated into phenotype. But the breadth of prion influences on biology and their evolutionary significance are just beginning to be explored. We report that a prion formed by the Mot3 transcription factor, [MOT3+], governs the acquisition of facultative multicellularity in the budding yeast Saccharomyces cerevisiae. The traits governed by [MOT3+] involved both gains and losses of Mot3 regulatory activity. [MOT3+]-dependent expression of FLO11, a major determinant of cell-cell adhesion, produced diverse lineage-specific multicellular phenotypes in response to nutrient deprivation. The prions themselves were induced by ethanol and eliminated by hypoxia—conditions that occur sequentially in the natural respiro-fermentative cycles of yeast populations. These data demonstrate that prions can act as environmentally responsive molecular determinants of multicellularity and contribute to the natural morphological diversity of budding yeast.PaperFlick

[GAR[superscript +]] is a protein-based element of inheritance that allows yeast (Saccharomyces cerevisiae) to circumvent a normal hallmark of their biology: extreme metabolic specialization for glucose fermentation. When glucose is present, even in trace quantities, yeast will not use other carbon sources. [GAR[superscript +]] allows cells to circumvent this “glucose repression.” [GAR[superscript +]] is induced in yeast by a factor secreted by bacteria inhabiting their environment. We report that the de novo rates of [GAR[superscript +]] appearance correlate with the yeast’s ecological niche. Evolutionarily distant fungi possess similar epigenetic elements that are also induced by bacteria. As expected for a mechanism whose adaptive value originates from the selective pressures of life in biological communities, the ability of bacteria to induce [GAR[superscript +]] and the ability of yeast to respond to bacterial signals have been extinguished repeatedly during the extended monoculture of domestication. Thus, [GAR[superscript +]] is a broadly conserved adaptive strategy that links environmental and social cues to heritable changes in metabolism., G. Harold and Leila Y. Mathers Foundation, Howard Hughes Medical Institute