Abstract
Robust preference for fermentative glucose metabolism has motivated domestication of the budding yeast Saccharomyces cerevisiae. This program can be circumvented by a protein-based genetic element, the [GAR+] prion, permitting simultaneous metabolism of glucose and other carbon sources. Diverse bacteria can elicit yeast cells to acquire [GAR+], although the molecular details of this interaction remain unknown. Here we identify the common bacterial metabolite lactic acid as a strong [GAR+] inducer. Transient exposure to lactic acid caused yeast cells to heritably circumvent glucose repression. This trait had the defining genetic properties of [GAR+], and did not require utilization of lactic acid as a carbon source. Lactic acid also induced [GAR+]-like epigenetic states in fungi that diverged from S. cerevisiae ~200 million years ago, and in which glucose repression evolved independently. To our knowledge, this is the first study to uncover a bacterial metabolite with the capacity to potently induce a prion.
Highlights
Small molecules commonly drive productive and destructive relationships between species
Pasteur and others since have noted that lactic acid bacteria are a common contaminant in incomplete fermentations (Boulton et al, 1996; Pasteur, 1873)
We recently reported that yeast strains have the ability to overcome such glucose-associated repression of metabolism at frequencies that depend upon the ecological niche from which they were isolated (Jarosz et al, 2014a, 2014b)
Summary
Small molecules commonly drive productive and destructive relationships between species. The breadth of these molecular messages is vividly illustrated by examples ranging from bacterial control of fungal pathogenesis to programming of multi-cellular development (Alegado et al, 2012; Ehrhardt et al, 1992; Hogan and Kolter, 2002; Hogan et al, 2004). Cross-kingdom interactions have commercial relevance – for example those that occur between yeast and bacteria in the fermentation of alcoholic beverages (Bisson et al, 2007; Bokulich et al, 2012; Boulton et al, 1996). Brewers and vintners have long appreciated that some bacteria have the power to both reduce the ethanol content and spoil the taste profile of fermented beverages
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