Abstract
Establishment of the [GAR+] prion in Saccharomyces cerevisiae reduces both transcriptional expression of the HXT3 hexose transporter gene and fermentation capacity in high sugar conditions. We evaluated the impact of deletion of the HXT3 gene on the expression of [GAR+] prion phenotype in a vineyard isolate, UCD932, and found that changes in fermentation capacity were observable even with complete loss of the Hxt3 transporter, suggesting other cellular functions affecting fermentation rate may be impacted in [GAR+] strains. In a comparison of isogenic [GAR+] and [gar–] strains, localization of the Pma1 plasma membrane ATPase showed differences in distribution within the membrane. In addition, plasma membrane lipid composition varied between the two cell types. Oxygen uptake was decreased in prion induced cells suggesting membrane changes affect plasma membrane functionality beyond glucose transport. Thus, multiple cell surface properties are altered upon induction of the [GAR+] prion in addition to changes in expression of the HXT3 gene. We propose a model wherein [GAR+] prion establishment within a yeast population is associated with modulation of plasma membrane functionality, fermentation capacity, niche dominance, and cell physiology to facilitate growth and mitigate cytotoxicity under certain environmental conditions. Down-regulation of expression of the HXT3 hexose transporter gene is only one component of a suite of physiological differences. Our data show the [GAR+] prion state is accompanied by multiple changes in the yeast cell surface that prioritize population survivability over maximizing metabolic capacity and enable progeny to establish an alternative adaptive state while maintaining reversibility.
Highlights
Saccharomyces cerevisiae is a remarkably adaptable organism specialized in dominating fermentative environments (Karpel et al, 2008; Bisson and Karpel, 2010)
To test the hypothesis that loss of hexose transporter 3 (HXT3) is responsible for this decrease in fermentation rate in [GAR+] wine yeast cells, fermentations with a UCD932 hxt3 null mutant were performed
The organic acids produced by bacteria, especially acetic acid (Ramakrishnan et al, 2016), are detrimental to yeast and, depending on the strain history/environmental niche, a portion of a population will induce the [GAR+] prion due to the disruption of cellular homeostasis (Ullah et al, 2013; Garcia et al, 2016; Ramakrishnan et al, 2016)
Summary
Saccharomyces cerevisiae is a remarkably adaptable organism specialized in dominating fermentative environments (Karpel et al, 2008; Bisson and Karpel, 2010). Proto-prion proteins contain intrinsically disordered domains that can spontaneously refold into the [PRION+] form in response to loss of cellular homeostasis (Garcia and Jarosz, 2014; Chakrabortee et al, 2016). Refolding of these domains in regulatory proteins constitutes a type of structural “switch” which leads to sequestration or differential associations, and can even confer novel functions to the target protein (Harvey et al, 2017). These epigenetic “switch” elements display characteristics of non-Mendelian inheritance
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