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Residual mitochondrial transmembrane potential decreases unsaturated fatty acid level in sake yeast during alcoholic fermentation.

ABSTRACT: Oxygen, a key nutrient in alcoholic fermentation, is rapidly depleted during this process. Several pathways of oxygen utilization have been reported in the yeast Saccharomyces cerevisiae during alcoholic fermentation, namely synthesis of unsaturated fatty acid, sterols and heme, and the mitochondrial electron transport chain. However, the interaction between these pathways has not been investigated. In this study, we showed that the major proportion of unsaturated fatty acids of ester-linked lipids in sake fermentation mash is derived from the sake yeast rather than from rice or koji (rice fermented with Aspergillus). Additionally, during alcoholic fermentation, inhibition of the residual mitochondrial activity of sake yeast increases the levels of unsaturated fatty acids of ester-linked lipids. These findings indicate that the residual activity of the mitochondrial electron transport chain reduces molecular oxygen levels and decreases the synthesis of unsaturated fatty acids, thereby increasing the synthesis of estery flavors by sake yeast. This is the first report of a novel link between residual mitochondrial transmembrane potential and the synthesis of unsaturated fatty acids by the brewery yeast during alcoholic fermentation.

SUBMITTER: Sawada K

PROVIDER: S-EPMC4734444 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Residual mitochondrial transmembrane potential decreases unsaturated fatty acid level in sake yeast during alcoholic fermentation.

Sawada Kazutaka K Kitagaki Hiroshi H

PeerJ 20160114

Oxygen, a key nutrient in alcoholic fermentation, is rapidly depleted during this process. Several pathways of oxygen utilization have been reported in the yeast Saccharomyces cerevisiae during alcoholic fermentation, namely synthesis of unsaturated fatty acid, sterols and heme, and the mitochondrial electron transport chain. However, the interaction between these pathways has not been investigated. In this study, we showed that the major proportion of unsaturated fatty acids of ester-linked lip ...[more]

PMID: 26839744

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Project description:The levels of unsaturated fatty acids (UFAs) in grape must significantly influence yeast metabolism and the production of aroma compounds. In this work, cDNA microarray technology was applied to analyze the transcriptional discrepancies of wine yeast (commercial wine yeast Lalvin EC1118) fermenting in synthetic grape must supplemented with different concentrations of a mixture of UFAs (including linoleic acid, oleic acid, and ?-linolenic acid). The results showed that the initial addition of a high level of UFAs can significantly enrich the intracellular UFAs when compared to a low addition of UFAs and further increase the cell population and most volatiles, including higher alcohols and esters, except for several fatty acids. Microarray analyses identified that 63 genes were upregulated, and 91 genes were downregulated during the different fermentation stages. The up-regulated genes were involved in yeast growth and proliferation, stress responses and amino acid transportation, while the repressed genes were associated with lipid and sterol biosynthesis, amino acid metabolism, TCA cycle regulation, mitochondrial respiration, and stress responses. Unexpectedly, the genes directly related to the biosynthesis of volatile compounds did not vary substantially between the fermentations with the high and low UFA additions. The beneficial aromatic function of the UFAs was ascribed to the increased biomass and amino acid transportation, considering that the incorporation of the additional UFAs in yeast cells maintains high membrane fluidity and increases the ability of the cells to resist deleterious conditions. Our results highlighted the importance of UFAs in the regulation of aroma biosynthesis during wine fermentation and suggested that the improvement of the resistance of yeast to extreme stresses during alcoholic fermentation is essential to effectively modulate and improve the production of aroma compounds. A potential way to achieve this goal could be the rational increase of the UFA contents in grape must.

Project description:Saccharomyces cerevisiae sake yeast strain Kyokai no. 7 (K7) and its relatives carry a homozygous loss-of-function mutation in the RIM15 gene, which encodes a Greatwall family protein kinase. Disruption of RIM15 in nonsake yeast strains leads to improved alcoholic fermentation, indicating that the defect in Rim15p is associated with the enhanced fermentation performance of sake yeast cells. In order to understand how Rim15p mediates fermentation control, we here focused on target-of-rapamycin protein kinase complex 1 (TORC1) and protein phosphatase 2A with the B55? regulatory subunit (PP2AB55?), complexes that are known to act upstream and downstream of Rim15p, respectively. Several lines of evidence, including our previous transcriptomic analysis data, suggested enhanced TORC1 signaling in sake yeast cells during sake fermentation. Fermentation tests of the TORC1-related mutants using a laboratory strain revealed that TORC1 signaling positively regulates the initial fermentation rate in a Rim15p-dependent manner. Deletion of the CDC55 gene, encoding B55?, abolished the high fermentation performance of Rim15p-deficient laboratory yeast and sake yeast cells, indicating that PP2AB55? mediates the fermentation control by TORC1 and Rim15p. The TORC1-Greatwall-PP2AB55? pathway similarly affected the fermentation rate in the fission yeast Schizosaccharomyces pombe, strongly suggesting that the evolutionarily conserved pathway governs alcoholic fermentation in yeasts. It is likely that elevated PP2AB55? activity accounts for the high fermentation performance of sake yeast cells. Heterozygous loss-of-function mutations in CDC55 found in K7-related sake strains may indicate that the Rim15p-deficient phenotypes are disadvantageous to cell survival.IMPORTANCE The biochemical processes and enzymes responsible for glycolysis and alcoholic fermentation by the yeast S. cerevisiae have long been the subject of scientific research. Nevertheless, the factors determining fermentation performance in vivo are not fully understood. As a result, the industrial breeding of yeast strains has required empirical characterization of fermentation by screening numerous mutants through laborious fermentation tests. To establish a rational and efficient breeding strategy, key regulators of alcoholic fermentation need to be identified. In the present study, we focused on how sake yeast strains of S. cerevisiae have acquired high alcoholic fermentation performance. Our findings provide a rational molecular basis to design yeast strains with optimal fermentation performance for production of alcoholic beverages and bioethanol. In addition, as the evolutionarily conserved TORC1-Greatwall-PP2AB55? pathway plays a major role in the glycolytic control, our work may contribute to research on carbohydrate metabolism in higher eukaryotes.

Dataset Information

Residual mitochondrial transmembrane potential decreases unsaturated fatty acid level in sake yeast during alcoholic fermentation.

Publications

Residual mitochondrial transmembrane potential decreases unsaturated fatty acid level in sake yeast during alcoholic fermentation.

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