Ethanol Production and Maximum Cell Growth Are Highly Correlated with Membrane Lipid Composition during Fermentation as Determined by Lipidomic Analysis of 22 Saccharomyces cerevisiae Strains

Henderson, Clark M.; Lozada-Contreras, Michelle; Jiranek, Vladimir; Longo, Marjorie L.; Block, David E.

doi:10.1128/aem.02670-12

Cited by 55 publications

(69 citation statements)

References 53 publications

(97 reference statements)

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“…S4). Taken together, these results are in accordance with the well-recognized actions of ethanol, i.e., perturbing the plasma membrane fluidity (63) and modifying the phospholipid and ergosterol content (17,69,70), thereby compromising the selectively permeable nature of the cell membrane.…”

Section: Resultssupporting

confidence: 71%

Evidence for a Role for the Plasma Membrane in the Nanomechanical Properties of the Cell Wall as Revealed by an Atomic Force Microscopy Study of the Response of Saccharomyces cerevisiae to Ethanol Stress

Schiavone

Formosa-Dague

Elsztein

et al. 2016

Appl Environ Microbiol

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A wealth of biochemical and molecular data have been reported regarding ethanol toxicity in the yeast Saccharomyces cerevisiae. However, direct physical data on the effects of ethanol stress on yeast cells are almost nonexistent. This lack of information can now be addressed by using atomic force microscopy (AFM) technology. In this report, we show that the stiffness of glucosegrown yeast cells challenged with 9% (vol/vol) ethanol for 5 h was dramatically reduced, as shown by a 5-fold drop of Young's modulus. Quite unexpectedly, a mutant deficient in the Msn2/Msn4 transcription factor, which is known to mediate the ethanol stress response, exhibited a low level of stiffness similar to that of ethanol-treated wild-type cells. Reciprocally, the stiffness of yeast cells overexpressing MSN2 was about 35% higher than that of the wild type but was nevertheless reduced 3-to 4-fold upon exposure to ethanol. Based on these and other data presented herein, we postulated that the effect of ethanol on cell stiffness may not be mediated through Msn2/Msn4, even though this transcription factor appears to be a determinant in the nanomechanical properties of the cell wall. On the other hand, we found that as with ethanol, the treatment of yeast with the antifungal amphotericin B caused a significant reduction of cell wall stiffness. Since both this drug and ethanol are known to alter, albeit by different means, the fluidity and structure of the plasma membrane, these data led to the proposition that the cell membrane contributes to the biophysical properties of yeast cells. IMPORTANCEEthanol is the main product of yeast fermentation but is also a toxic compound for this process. Understanding the mechanism of this toxicity is of great importance for industrial applications. While most research has focused on genomic studies of ethanol tolerance, we investigated the effects of ethanol at the biophysical level and found that ethanol causes a strong reduction of the cell wall rigidity (or stiffness). We ascribed this effect to the action of ethanol perturbing the cell membrane integrity and hence proposed that the cell membrane contributes to the cell wall nanomechanical properties. T he yeast Saccharomyces cerevisiae is a remarkable ethanol producer that is also very sensitive to its main fermentative product. At low to moderate concentrations (5 to 7%), ethanol mainly affects the growth rate, and at higher concentrations (Ͼ10%), it can strongly impair cell integrity, eventually leading to cell death with features of apoptosis (1). These inhibitory and toxic effects are ascribed to the fact that ethanol alters cell membrane fluidity and dissipates the transmembrane electrochemical potential, thereby creating permeability to ionic species and causing leakage of metabolites (2). Recent works using lipidomic methodologies confirmed the relationship between the composition of lipids, notably ergosterol and unsaturated fatty acids, and ethanol tolerance (3, 4). Moreover, as it diffuses freely into cells, ethanol at high concen...

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Section: Resultssupporting

confidence: 71%

Evidence for a Role for the Plasma Membrane in the Nanomechanical Properties of the Cell Wall as Revealed by an Atomic Force Microscopy Study of the Response of Saccharomyces cerevisiae to Ethanol Stress

Schiavone

Formosa-Dague

Elsztein

et al. 2016

Appl Environ Microbiol

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“…In particular, yeast strains that converted more sugar to ethanol had higher levels of specific phosphatidylcholine species that have previously been demonstrated to stabilize model membrane bilayers in a highethanol milieu (48). Strains that were unable to complete fermentation had higher concentrations of phosphatidylinositol during the early stages of fermentation (65). Interestingly, ergosterol was not significantly correlated with ethanol production or yeast cell growth, in agreement with the observations of previous studies analyzing yeast lipid composition during alcoholic fermentation (20,63,64).…”

Section: Lipid Composition In Yeast Alcoholic Fermentationssupporting

confidence: 81%

“…The results from this analysis confirmed that the fermentation temperature had a profound effect on fermentation kinetics and yeast cell lipid composition. Furthermore, these data revealed that stuck fermentations at high temperatures (35°C) and low-temperature fermentations (15°C) had significantly different lipid compositions (65). Specifically, all of the yeast strains analyzed in this study that experienced fermentation arrest at elevated temperatures had higher concentrations of several phosphatidylinositol species than at other temperatures.…”

Section: Lipid Composition In Yeast Alcoholic Fermentationsmentioning

confidence: 73%

“…Furthermore, none of the investigations discussed here provided structural data on the lipids, which would be critical to understanding how specific lipid species contribute to ethanol tolerance and to elucidate potential mechanisms by which the membrane mitigates the toxic effects of ethanol. Analyses of lipid compositional changes that occur during fermentation in numerous yeast strains with various levels of ethanol tolerance utilizing modern tools of lipidomics and chemometrics are providing much greater insight into how this organism's membrane adapts to ethanol (63)(64)(65). Recently, we developed an analytical methodology utilizing high-performance liquid chromatography coupled online to atmospheric pressure ionization mass spectrometry (API-MS) that facilitates rapid quantitative analysis of yeast lipid extracts (64).…”

Section: Lipid Composition In Yeast Alcoholic Fermentationsmentioning

confidence: 99%

“…Recently, we developed an analytical methodology utilizing high-performance liquid chromatography coupled online to atmospheric pressure ionization mass spectrometry (API-MS) that facilitates rapid quantitative analysis of yeast lipid extracts (64). This method was used in conjunction with multivariate statistical analysis to ascertain how the lipid composition in 22 Saccharomyces cerevisiae strains correlated with yeast cell growth and ethanol production over the course of alcoholic fermentation (65). Partial least-squares regression modeling of the correlation of the lipid composition data to fermentation kinetic data indicated that both ethanol production and maximum yeast cell density were highly correlated with yeast cell lipid composition.…”

Section: Lipid Composition In Yeast Alcoholic Fermentationsmentioning

confidence: 99%

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Examining the Role of Membrane Lipid Composition in Determining the Ethanol Tolerance of Saccharomyces cerevisiae

Henderson

Block

2014

Appl Environ Microbiol

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120

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Yeast (Saccharomyces cerevisiae) has an innate ability to withstand high levels of ethanol that would prove lethal to or severely impair the physiology of other organisms. Significant efforts have been undertaken to elucidate the biochemical and biophysical mechanisms of how ethanol interacts with lipid bilayers and cellular membranes. This research has implicated the yeast cellular membrane as the primary target of the toxic effects of ethanol. Analysis of model membrane systems exposed to ethanol has demonstrated ethanol's perturbing effect on lipid bilayers, and altering the lipid composition of these model bilayers can mitigate the effect of ethanol. In addition, cell membrane composition has been correlated with the ethanol tolerance of yeast cells. However, the physical phenomena behind this correlation are likely to be complex. Previous work based on often divergent experimental conditions and time-consuming low-resolution methodologies that limit large-scale analysis of yeast fermentations has fallen short of revealing shared mechanisms of alcohol tolerance in Saccharomyces cerevisiae. Lipidomics, a modern mass spectrometry-based approach to analyze the complex physiological regulation of lipid composition in yeast and other organisms, has helped to uncover potential mechanisms for alcohol tolerance in yeast. Recent experimental work utilizing lipidomics methodologies has provided a more detailed molecular picture of the relationship between lipid composition and ethanol tolerance. While it has become clear that the yeast cell membrane composition affects its ability to tolerate ethanol, the molecular mechanisms of yeast alcohol tolerance remain to be elucidated.

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Dynamic genome‐scale modeling of Saccharomyces cerevisiae unravels mechanisms for ester formation during alcoholic fermentation

Scott

Henriques

Smid

et al. 2023

Biotech & Bioengineering

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Fermentation employing Saccharomyces cerevisiae has produced alcoholic beverages and bread for millennia. More recently, S. cerevisiae has been used to manufacture specific metabolites for the food, pharmaceutical, and cosmetic industries. Among the most important of these metabolites are compounds associated with desirable aromas and flavors, including higher alcohols and esters. Although the physiology of yeast has been well‐studied, its metabolic modulation leading to aroma production in relevant industrial scenarios such as winemaking is still unclear. Here we ask what are the underlying metabolic mechanisms that explain the conserved and varying behavior of different yeasts regarding aroma formation under enological conditions? We employed dynamic flux balance analysis (dFBA) to answer this key question using the latest genome‐scale metabolic model (GEM) of S. cerevisiae. The model revealed several conserved mechanisms among wine yeasts, for example, acetate ester formation is dependent on intracellular metabolic acetyl‐CoA/CoA levels, and the formation of ethyl esters facilitates the removal of toxic fatty acids from cells using CoA. Species‐specific mechanisms were also found, such as a preference for the shikimate pathway leading to more 2‐phenylethanol production in the Opale strain as well as strain behavior varying notably during the carbohydrate accumulation phase and carbohydrate accumulation inducing redox restrictions during a later cell growth phase for strain Uvaferm. In conclusion, our new metabolic model of yeast under enological conditions revealed key metabolic mechanisms in wine yeasts, which will aid future research strategies to optimize their behavior in industrial settings.

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Ethanol Production and Maximum Cell Growth Are Highly Correlated with Membrane Lipid Composition during Fermentation as Determined by Lipidomic Analysis of 22 Saccharomyces cerevisiae Strains

Cited by 55 publications

References 53 publications

Evidence for a Role for the Plasma Membrane in the Nanomechanical Properties of the Cell Wall as Revealed by an Atomic Force Microscopy Study of the Response of Saccharomyces cerevisiae to Ethanol Stress

Evidence for a Role for the Plasma Membrane in the Nanomechanical Properties of the Cell Wall as Revealed by an Atomic Force Microscopy Study of the Response of Saccharomyces cerevisiae to Ethanol Stress

Examining the Role of Membrane Lipid Composition in Determining the Ethanol Tolerance of Saccharomyces cerevisiae

Dynamic genome‐scale modeling of Saccharomyces cerevisiae unravels mechanisms for ester formation during alcoholic fermentation

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