Lipidomic Profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii Reveals Critical Changes in Lipid Composition in Response to Acetic Acid Stress

Lindberg, Lina; Santos, Aline Xavier da Silveira dos; Riezman, Howard; Olsson, Lisbeth; Bettiga, Maurizio

doi:10.1371/journal.pone.0073936

Cited by 113 publications

(126 citation statements)

References 65 publications

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“…Accumulation of intracellular acetic acid and consequently acetic acid stress can thereby be avoided when v Diff and, if relevant, v Uptake is less than the sum of v Cons and v Ext . Indeed, a comparison of the acetic acid uptake rate (v Diff and v Uptake ) measured by Stratford et al (2013) and the acetic acid consumption rate (v Cons ) determined in our previous study (Lindberg et al, 2013) reveals that these rates are of the same order of magnitude, supporting our hypothesis that the diffusion rate is important in intracellular acetic acid accumulation and, hence, tolerance.…”

Section: Introductionsupporting

confidence: 86%

“…No direct comparison has been made of the acetic acid membrane permeability in Z. bailii and S. cerevisiae , but measurements of propionic acid uptake have shown that it is more than ten times faster in S. cerevisiae than in Z. bailii (Warth, 1989). In our previous study, we investigated the plasma membrane lipid profile of S. cerevisiae and Z. bailii , showing a strong difference in lipid profile between the two yeasts, with sphingolipids being several times higher in Z. bailii than in S. cerevisiae , supporting a potential difference in membrane permeability (Lindberg et al, 2013). In addition, Z. bailii showed a unique ability to remodel the composition of its plasma membrane upon acetic acid stress, so as to greatly increase the fraction of sphingolipids (two to nine times increase depending on sphingolipid class), at the expense of glycerophospholipids (overall level reduced by half and phosphatidyl inositol which is required for sphingolipid synthesis increased from 40 to 88% of the total glycerophospholipids in the membrane).…”

Section: Introductionmentioning

confidence: 91%

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Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii

Lindahl

Genheden

Eriksson

et al. 2015

Biotech & Bioengineering

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Lignocellulosic raw material plays a crucial role in the development of sustainable processes for the production of fuels and chemicals. Weak acids such as acetic acid and formic acid are troublesome inhibitors restricting efficient microbial conversion of the biomass to desired products. To improve our understanding of weak acid inhibition and to identify engineering strategies to reduce acetic acid toxicity, the highly acetic‐acid‐tolerant yeast Zygosaccharomyces bailii was studied. The impact of acetic acid membrane permeability on acetic acid tolerance in Z. bailii was investigated with particular focus on how the previously demonstrated high sphingolipid content in the plasma membrane influences acetic acid tolerance and membrane permeability. Through molecular dynamics simulations, we concluded that membranes with a high content of sphingolipids are thicker and more dense, increasing the free energy barrier for the permeation of acetic acid through the membrane. Z. bailii cultured with the drug myriocin, known to decrease cellular sphingolipid levels, exhibited significant growth inhibition in the presence of acetic acid, while growth in medium without acetic acid was unaffected by the myriocin addition. Furthermore, following an acetic acid pulse, the intracellular pH decreased more in myriocin‐treated cells than in control cells. This indicates a higher inflow rate of acetic acid and confirms that the reduction in growth of cells cultured with myriocin in the medium with acetic acid was due to an increase in membrane permeability, thereby demonstrating the importance of a high fraction of sphingolipids in the membrane of Z. bailii to facilitate acetic acid resistance; a property potentially transferable to desired production organisms suffering from weak acid stress. Biotechnol. Bioeng. 2016;113: 744–753. © 2015 The Authors. Biotechnology and Bioengineering Published by Wiley Periodicals, Inc.

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Section: Introductionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 91%

Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii

Lindahl

Genheden

Eriksson

et al. 2015

Biotech & Bioengineering

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“…Extensive remodeling of Saccharomyces cerevisiae cell envelope has been described to occur in response to acetic acid stress, this aiming to reduce the rate by which acetic acid diffuses to the cell interior (Ullah et al 2013). These alterations include both alterations of the cell wall structure (Simões et al 2006) and of the lipid composition of the plasma membrane (Lindberg et al 2013). The increase in the rate of endocytosis of the Fps1 channel (Mollapour and Piper 2007) is another mechanism by which yeast cells reduce the entry of acetic acid.…”

Section: Toxic Effect Of Acetic Acid In Yeast Cells and Underlying Admentioning

confidence: 99%

Adaptation and tolerance of bacteria against acetic acid

Trček

Mira

Jarboe

2015

Appl Microbiol Biotechnol

188

100

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Acetic acid is a weak organic acid exerting a toxic effect to most microorganisms at concentrations as low as 0.5 wt%. This toxic effect results mostly from acetic acid dissociation inside microbial cells, causing a decrease of intracellular pH and metabolic disturbance by the anion, among other deleterious effects. These microbial inhibition mechanisms enable acetic acid to be used as a preservative, although its usefulness is limited by the emergence of highly tolerant spoilage strains. Several biotechnological processes are also inhibited by the accumulation of acetic acid in the growth medium including production of bioethanol from lignocellulosics, wine making, and microbe-based production of acetic acid itself. To design better preservation strategies based on acetic acid and to improve the robustness of industrial biotechnological processes limited by this acid's toxicity, it is essential to deepen the understanding of the underlying toxicity mechanisms. In this sense, adaptive responses that improve tolerance to acetic acid have been well studied in Escherichia coli and Saccharomyces cerevisiae. Strains highly tolerant to acetic acid, either isolated from natural environments or specifically engineered for this effect, represent a unique reservoir of information that could increase our understanding of acetic acid tolerance and contribute to the design of additional tolerance mechanisms. In this article, the mechanisms underlying the acetic acid tolerance exhibited by several bacterial strains are reviewed, with emphasis on the knowledge gathered in acetic acid bacteria and E. coli. A comparison of how these bacterial adaptive responses to acetic acid stress fit to those described in the yeast Saccharomyces cerevisiae is also performed. A systematic comparison of the similarities and dissimilarities of the ways by which different microbial systems surpass the deleterious effects of acetic acid toxicity has not been performed so far, although such exchange of knowledge can open the door to the design of novel approaches aiming the development of acetic acid-tolerant strains with increased industrial robustness in a synthetic biology perspective.

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“…The yeast S. cerevisiae has developed several mechanisms by which it can counteract the harmful effects that acetic acid exerts on the cells. In general, adaptation to acetic acid has been associated with the abilities to recover intracellular pH (3,(9)(10)(11), to inhibit further uptake of acetic acid (12), to activate multidrug transporters to pump out acetate anions (3,13), and to adjust the membrane lipid profile (14). Among these mechanisms, recovery of intracellular pH is thought to be of predominant importance in the responses of S. cerevisiae to acetic acid (9).…”

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confidence: 99%

The Cytosolic pH of Individual Saccharomyces cerevisiae Cells Is a Key Factor in Acetic Acid Tolerance

Fernández-Niño

Marquina

Swinnen

et al. 2015

Appl Environ Microbiol

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bIt was shown recently that individual cells of an isogenic Saccharomyces cerevisiae population show variability in acetic acid tolerance, and this variability affects the quantitative manifestation of the trait at the population level. In the current study, we investigated whether cell-to-cell variability in acetic acid tolerance could be explained by the observed differences in the cytosolic pHs of individual cells immediately before exposure to the acid. Results obtained with cells of the strain CEN.PK113-7D in synthetic medium containing 96 mM acetic acid (pH 4.5) showed a direct correlation between the initial cytosolic pH and the cytosolic pH drop after exposure to the acid. Moreover, only cells with a low initial cytosolic pH, which experienced a less severe drop in cytosolic pH, were able to proliferate. A similar correlation between initial cytosolic pH and cytosolic pH drop was also observed in the more acid-tolerant strain MUCL 11987-9. Interestingly, a fraction of cells in the MUCL 11987-9 population showed initial cytosolic pH values below the minimal cytosolic pH detected in cells of the strain CEN.PK113-7D; consequently, these cells experienced less severe drops in cytosolic pH. Although this might explain in part the difference between the two strains with regard to the number of cells that resumed proliferation, it was observed that all cells from strain MUCL 11987-9 were able to proliferate, independently of their initial cytosolic pH. Therefore, other factors must also be involved in the greater ability of MUCL 11987-9 cells to endure strong drops in cytosolic pH.T he study of microbial acetic acid tolerance is relevant in different fields of applied microbiology. Acetic acid, like other weak acids, such as sorbic acid and lactic acid, traditionally has been used as a preservative agent in food and beverages, where it prevents microbial spoilage by arresting the growth of yeasts and other fungi (1). However, certain strains of the species Zygosaccharomyces bailii and Saccharomyces cerevisiae still grow in the presence of relatively highly weak acid concentrations (2, 3), and, therefore, it is crucial to understand the underlying tolerance mechanisms in order to avoid food spoilage more effectively. More recently, understanding acetic acid tolerance of the platform yeast S. cerevisiae became important in the field of industrial biotechnology once hydrolysates of lignocellulosic biomass were considered renewable feedstock for microbial fermentations (4). Notably, the acetic acid concentrations in those hydrolysates can reach up to 133 mM (8 g liter Ϫ1 ) (5-7), at which the acid becomes a strong inhibitor of microbial growth and fermentation, especially at the low medium pH values typically used in industrial batch fermentations. Therefore, an understanding of the molecular mechanisms underlying S. cerevisiae tolerance to acetic acid is important for the generation of robust industrial strains that are able to ferment lignocellulosic hydrolysates efficiently.The inhibitory effect of acetic acid i...

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Lipidomic Profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii Reveals Critical Changes in Lipid Composition in Response to Acetic Acid Stress

Cited by 113 publications

References 65 publications

Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii

Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii

Adaptation and tolerance of bacteria against acetic acid

The Cytosolic pH of Individual Saccharomyces cerevisiae Cells Is a Key Factor in Acetic Acid Tolerance

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