The fraction of cells that resume growth after acetic acid addition is a strain-dependent parameter of acetic acid tolerance in<i>Saccharomyces cerevisiae</i>

Swinnen, Steve; Fernández-Niño, Miguel; González-Ramos, Daniel; Maris, Antonius J. A. van; Nevoigt, Elke

doi:10.1111/1567-1364.12151

Cited by 44 publications

(47 citation statements)

References 61 publications

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“…In a previous study, it was shown that only a fraction of cells in an S. cerevisiae population resumed proliferation upon exposure to acetic acid (20). This effect was observed in several strains that were exposed to a relatively high acetic acid concentration (157 mM acetic acid at pH 4.5).…”

Section: Resultsmentioning

confidence: 91%

“…Cells of the strain CEN.PK113-7D were therefore spread on solid synthetic medium containing acetic acid at concentrations ranging from 20 to 160 mM. This quantification method was demonstrated previously to represent properly the fraction of cells able to resume proliferation in liquid acetic acid-containing medium (20). Data showed that all cells (4 ϫ 10 6 CFU ml Ϫ1 ) were able to proliferate in the presence of the acid at concentrations of up to 80 mM (Fig.…”

Section: Resultsmentioning

confidence: 91%

“…A frequently reported effect is significant prolongation of the latency phase in the presence of inhibitory acetic acid concentrations (20)(21)(22)(23). This effect was demonstrated recently to be attributable to the fact that only a relatively small fraction of cells in the entire population are able to resume proliferation in the presence of acetic acid (20).…”

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confidence: 98%

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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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Section: Resultsmentioning

confidence: 91%

Section: Resultsmentioning

confidence: 91%

mentioning

confidence: 98%

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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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“…A large-scale chemical genomics study identified 648 genes whose deletion increased the susceptibility of yeast to acetic acid, and these gene determinants were found to be involved in carbohydrate metabolism, cell wall assembly, amino acid metabolism, internal pH homeostasis, biogenesis of mitochondria, and signaling and uptake of various nutrients (26). Recent studies reported cell-to-cell heterogeneity in acetic acid tolerance (28,29). It was found that only a fraction of the cells within an isogenic S. cerevisiae population resumed growth under acetic acid stress (28) and that variations in the cytosolic pH of individual cells might contribute to the differences between cells (29).…”

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confidence: 99%

“…Recent studies reported cell-to-cell heterogeneity in acetic acid tolerance (28,29). It was found that only a fraction of the cells within an isogenic S. cerevisiae population resumed growth under acetic acid stress (28) and that variations in the cytosolic pH of individual cells might contribute to the differences between cells (29). The findings suggested that genes related to cell-to-cell heterogeneity might be a potential pool for the search of genetic targets for improving acetic acid resistance.…”

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Improved Acetic Acid Resistance in Saccharomyces cerevisiae by Overexpression of the WHI2 Gene Identified through Inverse Metabolic Engineering

Chen

Stabryla

Wei

2016

Appl Environ Microbiol

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bDevelopment of acetic acid-resistant Saccharomyces cerevisiae is important for economically viable production of biofuels from lignocellulosic biomass, but the goal remains a critical challenge due to limited information on effective genetic perturbation targets for improving acetic acid resistance in the yeast. This study employed a genomic-library-based inverse metabolic engineering approach to successfully identify a novel gene target, WHI2 (encoding a cytoplasmatic globular scaffold protein), which elicited improved acetic acid resistance in S. cerevisiae. Overexpression of WHI2 significantly improved glucose and/or xylose fermentation under acetic acid stress in engineered yeast. The WHI2-overexpressing strain had 5-times-higher specific ethanol productivity than the control in glucose fermentation with acetic acid. Analysis of the expression of WHI2 gene products (including protein and transcript) determined that acetic acid induced endogenous expression of Whi2 in S. cerevisiae. Meanwhile, the whi2⌬ mutant strain had substantially higher susceptibility to acetic acid than the wild type, suggesting the important role of Whi2 in the acetic acid response in S. cerevisiae. Additionally, overexpression of WHI2 and of a cognate phosphatase gene, PSR1, had a synergistic effect in improving acetic acid resistance, suggesting that Whi2 might function in combination with Psr1 to elicit the acetic acid resistance mechanism. These results improve our understanding of the yeast response to acetic acid stress and provide a new strategy to breed acetic acid-resistant yeast strains for renewable biofuel production. Lignocellulosic biomass from nonfood stocks such as agricultural and forestry residues has been identified as the prime source for production of renewable biofuels to substitute for conventional fossil fuels in the face of growing demand for energy and rising concerns about greenhouse gas emissions (1-4). Bioconversion of plant cell wall materials by microbial fermentation is typically preceded by harsh (physico)chemical hydrolysis designed to release sugars; this hydrolysis treatment also generates by-products that are toxic to fermenting microorganisms (5, 6). Since hemicellulose and lignin in the plant cell wall are ubiquitously acetylated (7,8), the typical acidic pretreatment of lignocellulosic biomass generates substantial amounts of acetic acid (with concentrations ranging from 1 g/liter to 15 g/liter) in the resulting hydrolysates (9, 10). Acetic acid severely inhibits cell growth and fermentation activity in Saccharomyces cerevisiae (5, 6, 11-13), the predominant microorganism used in industrial fermentation (14, 15). Therefore, improvement in S. cerevisiae resistance to acetic acid is highly desired and critical for achieving efficient and economically viable bioconversion of cellulosic sugars to biofuels.The toxic effects of acetic acid in S. cerevisiae have been intensively characterized, and toxicity mechanisms have been proposed (10,11,(16)(17)(18)(19)(20). When the external pH is lower than the...

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Microbioreactor Systems for Accelerated Bioprocess Development

Hemmerich

Noack

Wiechert

et al. 2018

Biotechnology Journal

135

143

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In recent years, microbioreactor (MBR) systems have evolved towards versatile bioprocess engineering tools. They provide a unique solution to combine higher experimental throughput with extensive bioprocess monitoring and control, which is indispensable to develop economically and ecologically competitive bioproduction processes. MBR systems are based either on down-scaled stirred tank reactors or on advanced shaken microtiter plate cultivation devices. Importantly, MBR systems make use of optical measurements for non-invasive, online monitoring of important process variables like biomass concentration, dissolved oxygen, pH, and fluorescence. The application range of MBR systems can be further increased by integration into liquid handling robots, enabling automatization and, thus standardization, of various handling and operation procedures. Finally, the tight integration of quantitative strain phenotyping with bioprocess development under industrially relevant conditions greatly increases the probability of finding the right combination of producer strain and bioprocess control strategy. This review will discuss the current state of the art in the field of MBR systems and we can readily conclude that their importance for industrial biotechnology will further increase in the near future.

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The fraction of cells that resume growth after acetic acid addition is a strain-dependent parameter of acetic acid tolerance inSaccharomyces cerevisiae

Cited by 44 publications

References 61 publications

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

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

Improved Acetic Acid Resistance in Saccharomyces cerevisiae by Overexpression of the WHI2 Gene Identified through Inverse Metabolic Engineering

Microbioreactor Systems for Accelerated Bioprocess Development

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