Membrane fluidification by ethanol stress activates unfolded protein response in yeasts

Navarro-Tapia, Elisabet; Querol, Amparo; Pérez‐Torrado, Roberto

doi:10.1111/1751-7915.13032

Cited by 42 publications

(34 citation statements)

References 57 publications

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“…Ethanol tolerance is a complex phenotype, and different mechanisms may lead to improved tolerance. Fluidisation of the yeast membranes by ethanol is also known to activate the unfolded protein response (UPR), and it is speculated that a better response could lead to greater on April 4, 2021 by guest http://aem.asm.org/ Downloaded from tolerance (52). Moreover, yeast cells can increase their tolerance to ethanol by other mechanisms, such as the increase the biosynthesis of some amino acids, as tryptophan (53) and trehalose accumulation (54).…”

Section: Discussionmentioning

confidence: 99%

Lipid Composition Analysis Reveals Mechanisms of Ethanol Tolerance in the Model YeastSaccharomyces cerevisiae

Lairón-Peris

Routledge

Linney

et al. 2021

Appl Environ Microbiol

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Saccharomyces cerevisiae is an important unicellular yeast species within the biotechnological and food and beverage industries. A significant application of this species is the production of ethanol, where concentrations are limited by cellular toxicity, often at the level of the cell membrane. Here, we characterize 61 S. cerevisiae strains for ethanol tolerance and further analyse five representatives with varying ethanol tolerances. The most tolerant strain, AJ4, was dominant in co-culture at 0% and 10% ethanol. Unexpectedly, although it does not have the highest NIC or MIC, MY29 was the dominant strain in co-culture at 6% ethanol, which may be linked to differences in its basal lipidome. Whilst relatively few lipidomic differences were observed between strains, a significantly higher PE concentration was observed in the least tolerant strain, MY26, at 0% and 6% ethanol compared to the other strains that became more similar at 10%, indicating potential involvement of this lipid with ethanol sensitivity. Our findings reveal that AJ4 is best able to adapt its membrane to become more fluid in the presence of ethanol and lipid extracts from AJ4 also form the most permeable membranes. Furthermore, MY26 is least able to modulate fluidity in response to ethanol and membranes formed from extracted lipids are least leaky at physiological ethanol concentrations. Overall, these results reveal a potential mechanism of ethanol tolerance and suggests a limited set of membrane compositions that diverse yeast species use to achieve this. Importance Many microbial processes are not implemented at the industrial level because the product yield is poorer and more expensive than can be achieved by chemical synthesis. It is well established that microbes show stress responses during bioprocessing, and one reason for poor product output from cell factories is production conditions that are ultimately toxic to the cells. During fermentative processes, yeast cells encounter culture media with high sugar content, which is later transformed into high ethanol concentrations. Thus, ethanol toxicity is one of the major stresses in traditional and more recent biotechnological processes. We have performed a multilayer phenotypic and lipidomic characterization of a large number of industrial and environmental strains of Saccharomyces to identify key resistant and non-resistant isolates for future applications.

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Section: Discussionmentioning

confidence: 99%

Lipid Composition Analysis Reveals Mechanisms of Ethanol Tolerance in the Model YeastSaccharomyces cerevisiae

Lairón-Peris

Routledge

Linney

et al. 2021

Appl Environ Microbiol

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“…Physical and chemical factors affecting protein functions will affect the activity of enzymes; for example, high temperatures, strong acids, and strong bases can cause a loss of catalytic ability. Studies on other strains have shown that increased temperatures and other stresses (for example, ethanol stress) could lead to a number of changes, including protein denaturation, DNA damage, cell cycle arrest, and changes in the fluidity of the membrane 33 . One of the most deleterious factors in stressed cells is the disturbance (unfolding) of the protein structure, which leads to protein aggregation, thus affecting the functionality 34 .…”

Section: Discussionmentioning

confidence: 99%

Screening and evaluation of Monascus purpureusFJMR24 for enhancing the raw material utilization rate in rice wine brewing

Ren

Lin

et al. 2020

J Sci Food Agric

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BACKGROUND The rapid development of the rice wine industry has increased the demand for raw materials worldwide. A fungal strain with good adaptability to rice wine brewing conditions, which can also enhance the utilization rate of raw materials (URRM), thus increasing the production efficiency, was sought in the present research. RESULTS The strain FJMR24 was successfully isolated and screened from 35 fermentation starters and exhibited high amylase activity (2200.9 ± 18.5 U g−1) and high glucoamylase activity (2330.4 ± 31.9 U g−1). Based on a morphological examination and a sequence analysis of the internal transcribed spacer (ITS) gene and β‐tubulin gene, FJMR24 was identified as Monascus purpureus, which is an edible and versatile fungus that plays a dominant role in the processing of Hong Qu. A moderate pH of 5–6 under incubation at 35 °C for 5–6 days was favorable for the growth and enzyme production of FJMR24. The strain could also tolerate the extreme conditions of 15–45 °C, 18% ethanol (v/v), and an acidity of pH 2. The excellent fermentation adaptability of FJMR24 might enable it to retain high enzyme activity during rice wine brewing. As a result of the action of FJMR24, the URRM of the base liquor increased by around 26% due to increased starch hydrolysis efficiency, which was mainly due to the high unit enzyme activity of FJMR24. CONCLUSION This study provides perspectives for the application of a M. purpureus strain with high starch hydrolysis activity for enhancing the URRM in traditional rice wine brewing. © 2020 Society of Chemical Industry

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“…Unfortunately, little is known about how lipids modulate various biological mechanisms in yeast cells during beer fermentation besides affecting membrane structure and/or permeability. However, it is known that membrane fluidification by ethanol can activate the endoplasmic reticulum (ER)-5 linked unfolded protein response (UPR) (Navarro-Tapia et al, 2018) and lipids may have other roles in proteostasis, such as the removal of unfolded proteins from the ER by lipid droplets (LDs) (Vevea et al, 2015). LDs are important and highly dynamic cytoplasmic organelles that connect different parts of the cell, including the ER (Jacquier et al, 2011), mitochondria (Pu et al, 2011), peroxisomes (Kohlwein et al, 2013), and vacuoles (Barbosa et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Rethinking the role of lipids in lager yeast cells during beer fermentation from a transcriptome and systems biology perspective

Bonatto

2020

Preprint

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Brewing lager yeasts (Saccharomyces pastorianus) should deal with stressful conditions during beer fermentation, including ethanol toxicity. In response to ethanol toxicity, different biological mechanisms are modulated, including lipid biosynthesis. It is well known that during beer fermentation, the composition of yeast membranes change in response to ethanol toxicity, making it less fluid and permeable. Additionally, neutral lipids and lipid droplets (LDs) are produced in response to ethanol toxicity. LDs are membranous organelles that transport lipids and proteins, acting as a hub for inter-organellar communication and module the activity of mechanisms necessary for ethanol tolerance, like proteostasis and autophagy. Unfortunately, little is known about the interplay of lipid biosynthesis, proteostasis, and autophagy in lager cells during beer fermentation. Thus, a transcriptome single and meta-analysis using publically available DNA microarray data of lager yeast cells in conditions of beer fermentation and cell biomass propagation was used to select all the upregulated genes associated to autophagy, lipid biosynthesis, and proteostasis (ALP) during beer fermentation. Following transcriptome data collection, a top-down systems biology analyses was applied with the design of an ALP-associated shortest pathway protein-protein network (ALP network), selection of central nodes and communities within ALP network, and the observation of the overrepresented biological processes and cellular components by gene ontology (GO) analysis. The transcriptome results show the upregulation of 204 non redundant ALP genes in conditions of beer fermentation, whose respective proteins interact in a shortest pathway ALP network. Thirteen communities where selected from ALP network containing overrepresented processes and components like mitophagy, cytoplasm-to-vacuole transport, pieacemeal micrautophagy of the nucleus, endoplasmic reticulum (ER) stress, ergosterol and lipid biosynthesis, LDs, ER membrane, phagophore assembly, among others. These results indicated that ethanol tolerance in lager yeasts could be due to the modulation of proteostasis and different forms 2 of autophagy by lipid biosynthesis and LDs, and thus extending the importance of lipids for beer fermentation.

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Membrane fluidification by ethanol stress activates unfolded protein response in yeasts

Cited by 42 publications

References 57 publications

Lipid Composition Analysis Reveals Mechanisms of Ethanol Tolerance in the Model YeastSaccharomyces cerevisiae

Lipid Composition Analysis Reveals Mechanisms of Ethanol Tolerance in the Model YeastSaccharomyces cerevisiae

Screening and evaluation of Monascus purpureusFJMR24 for enhancing the raw material utilization rate in rice wine brewing

Rethinking the role of lipids in lager yeast cells during beer fermentation from a transcriptome and systems biology perspective

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