Abstract
To thrive in an ever-changing environment, microbes must widely distribute their progeny to colonize new territory. Simultaneously, they must evolve and adapt to the stresses of unpredictable surroundings. In both of these regards, diversity is key—if an entire population moved together or responded to the environment in the same way, it could easily go extinct. Here, we show that the epigenetic prion switch [SWI+] establishes a specialized subpopulation with a “pioneer” phenotypic program in Saccharomyces cerevisiae. Cells in the pioneer state readily disperse in water, enabling them to migrate and colonize new territory. Pioneers are also more likely to find and mate with genetically diverse partners, as inhibited mating-type switching causes mother cells to shun their own daughters. In the nonprion [swi−] state, cells instead have a “settler” phenotype, forming protective flocs and tending to remain in their current position. Settler cells are better able to withstand harsh conditions like drought and alkaline pH. We propose that these laboratory observations reveal a strategy employed in the wild to rapidly diversify and grant distinct, useful roles to cellular subpopulations that benefit the population as a whole.
Highlights
Microbes face a constant struggle for resources and survival in an environment that changes by the hour
In baker’s yeast, prion switching allows cells to acquire new states that may each be better adapted to different environments
We show that a particular yeast prion called [SWI+] enhances the ability of cells to disperse in flowing water and favors mating with dissimilar partners, promoting genetic diversification
Summary
Microbes face a constant struggle for resources and survival in an environment that changes by the hour. Severe drought, and other environmental factors can cause mass extinction events, leaving vast regions for surviving cells to recolonize. Likewise, events such as floods or fruit falling from trees may fill new areas with nutrients, enabling expansion and growth of microbial populations. Prions are powerful evolutionary devices by which yeast cells switch between phenotypic programs, “hedging their bets” to survive in fluctuating and unpredictable environments [1– 6]. A cell will generally contain one conformation for each prion protein, and these conformational states switch at rates that range from 10−2 to 10−7 cells per generation [2]. The combination of potential prion states can lead to a plethora of switchable phenotypes
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