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Extreme osmotolerance and halotolerance in food-relevant yeasts and the role of glycerol-dependent cell individuality

Stratford, Malcolm; Steels, Hazel; Novodvorska, Michaela; Archer, David B.; Avery, Simon V.


Malcolm Stratford

Hazel Steels

Michaela Novodvorska

David B. Archer

Professor of Eukaryotic Microbiology


Osmotolerance and halotolerance are used to describe resistance to sugars and salt, respectively. Here, a comprehensive screen of more than 600 different yeast isolates revealed that osmosensitive species were equally affected by NaCl and glucose. However, the relative toxicity of salt became increasingly prominent in more osmoresistant species. We confirmed that growth inhibition by glucose in a laboratory strain of Saccharomyces cerevisiae occurred at a lower water activity (Aw) than by salt (NaCl), and pre-growth in high levels of glucose or salt gave enhanced cross-resistance to either. Salt toxicity was largely due to osmotic stress but with an additive enhancement due to effects of the relevant cation. Almost all of the yeast isolates from the screen were also noted to exhibit hetero-resistance to both salt and sugar, whereby high concentrations restricted growth to a small minority of cells within the clonal populations. Rare resistant colonies required growth for up to 28 days to become visible. This cell individuality was more marked with salt than sugar, a possible further reflection of the ion toxicity effect. In both cases, heteroresistance in S. cerevisiae was strikingly dependent on the GPD1 gene product, important for glycerol synthesis. In contrast, a tps1? deletant impaired for trehalose showed altered MIC but no change in heteroresistance. Effects on heteroresistance were evident in chronic (but not acute) salt or glucose stress, particularly relevant to growth on low Aw foods. The study reports diverse osmotolerance and halotolerance phenotypes and heteroresistance across an extensive panel of yeast isolates, and indicates that Gpd1-dependent glycerol synthesis is a key determinant enabling growth of rare yeast subpopulations at low Aw, brought about by glucose and in particular salt.


Stratford, M., Steels, H., Novodvorska, M., Archer, D. B., & Avery, S. V. (2019). Extreme osmotolerance and halotolerance in food-relevant yeasts and the role of glycerol-dependent cell individuality. Frontiers in Microbiology, 9, 1-14.

Journal Article Type Article
Acceptance Date Dec 13, 2018
Online Publication Date Jan 9, 2019
Publication Date Jan 9, 2019
Deposit Date Jan 4, 2019
Publicly Available Date Jan 9, 2019
Journal Frontiers in Microbiology
Electronic ISSN 1664-302X
Publisher Frontiers Media
Peer Reviewed Peer Reviewed
Volume 9
Article Number 3238
Pages 1-14
Keywords Population diversity; Tps1; resistant sub-population; HOG pathway bet-hedging
Public URL
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