Abstract
During the fermentation of sake, cells of Saccharomyces cerevisiae are exposed to high concentrations of ethanol, thereby damaging the cell membrane and functional proteins. L-proline protects yeast cells from damage caused by freezing or oxidative stress. In this study, we evaluated the role of intracellular L-proline in cells of S. cerevisiae grown under ethanol stress. An L-proline-accumulating laboratory strain carries a mutant allele of PRO1, pro1(D154N), which encodes the Asp154Asn mutant gamma-glutamyl kinase. This mutation increases the activity of gamma-glutamyl kinase and gamma-glutamyl phosphate reductase, which catalyze the first two steps of L-proline synthesis and which together may form a complex in vivo. When cultured in liquid medium in the presence of 9% and 18% ethanol under static conditions, the cell viability of the L-proline-accumulating laboratory strain is greater than the cell viability of the parent strain. This result suggests that intracellular accumulation of L-proline may confer tolerance to ethanol stress. We constructed a novel sake yeast strain by disrupting the PUT1 gene, which is required for L-proline utilization, and replacing the wild-type PRO1 allele with the pro1(D154N) allele. The resultant strain accumulated L-proline and was more tolerant to ethanol stress than was the control strain. We used the strain that could accumulate L-proline to brew sake containing five times more L-proline than what is found in sake brewed with the control strain, without affecting the fermentation profiles.
MeSH Terms
Cell Survival/drug effects
Ethanol/metabolism,pharmacology
Genotype
Japan
Kinetics
Molecular Sequence Data
Oxidative Stress/drug effects
Plasmids
Proline/pharmacology
Saccharomyces cerevisiae/drug effects,genetics,physiology
Wine
Chemicals
Ethanol
Proline
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Takagi Hiroshi
Department of Bioscience, Fukui Prefectural University, 4-1-1 Kenjojima, Matsuoka-cho, Fukui 910-1195, Japan.
[email protected]
Takaoka Miki
Kawaguchi Akari
Kubo Yoshito
References (29)
29 references, click to expand
-
Effect of gene disruption of succinate dehydrogenase on succinate production in a sake yeast strain.
J Biosci Bioeng. 2000;90(6):619-24
PMID: 16232921
-
Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline.
Cryobiology. 1985 Aug;22(4):367-77
PMID: 4028782
-
Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants.
Plant Physiol. 1995 Aug;108(4):1387-1394
PMID: 12228549
-
Proline is a protein solubilizing solute.
Biochem Mol Biol Int. 1997 Feb;41(2):235-42
PMID: 9063563
-
Proline utilization in Saccharomyces cerevisiae: analysis of the cloned PUT1 gene.
Mol Cell Biol. 1986 Jul;6(7):2638-45
PMID: 3537723
-
Proline utilization in Saccharomyces cerevisiae: analysis of the cloned PUT2 gene.
Mol Cell Biol. 1983 Oct;3(10):1846-56
PMID: 6358862
-
Isolation of freeze-tolerant laboratory strains of Saccharomyces cerevisiae from proline-analogue-resistant mutants.
Appl Microbiol Biotechnol. 1997 Apr;47(4):405-11
PMID: 9163955
-
Ethanol and the fluidity of the yeast plasma membrane.
Yeast. 1987 Dec;3(4):223-32
PMID: 3332975
-
In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast.
Methods Enzymol. 1991;194:302-18
PMID: 2005795
-
Gene dosage effect of L-proline biosynthetic enzymes on L-proline accumulation and freeze tolerance in Saccharomyces cerevisiae.
Appl Environ Microbiol. 2003 Nov;69(11):6527-32
PMID: 14602584
-
Gene-enzyme relationships in the proline biosynthetic pathway of Saccharomyces cerevisiae.
J Bacteriol. 1987 Dec;169(12):5364-72
PMID: 2824433
-
Proline inhibits aggregation during protein refolding.
Protein Sci. 2000 Feb;9(2):344-52
PMID: 10716186
-
Effect of proline and arginine metabolism on freezing stress of Saccharomyces cerevisiae.
J Biosci Bioeng. 2002;94(5):390-4
PMID: 16233323
-
Genetics and physiology of proline utilization in Saccharomyces cerevisiae: enzyme induction by proline.
J Bacteriol. 1979 Nov;140(2):498-503
PMID: 387737
-
Isolation of sake yeast strains possessing various levels of succinate- and/or malate-producing abilities by gene disruption or mutation.
J Biosci Bioeng. 1999;87(3):333-9
PMID: 16232477
-
Physiological and genetic responses of bacteria to osmotic stress.
Microbiol Rev. 1989 Mar;53(1):121-47
PMID: 2651863
-
L-proline accumulation and freeze tolerance of Saccharomyces cerevisiae are caused by a mutation in the PRO1 gene encoding gamma-glutamyl kinase.
Appl Environ Microbiol. 2003 Jan;69(1):212-9
PMID: 12513997
-
A role of Saccharomyces cerevisiae fatty acid activation protein 4 in palmitoyl-CoA pool for growth in the presence of ethanol.
J Biosci Bioeng. 2002;93(3):288-95
PMID: 16233202
-
Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae.
FEBS Lett. 2001 Jun 1;498(1):98-103
PMID: 11389906
-
Proline accumulation by mutation or disruption of the proline oxidase gene improves resistance to freezing and desiccation stresses in Saccharomyces cerevisiae.
FEMS Microbiol Lett. 2000 Mar 1;184(1):103-8
PMID: 10689174
-
Genetic engineering of a sake yeast producing no urea by successive disruption of arginase gene.
Appl Environ Microbiol. 1991 Jan;57(1):301-6
PMID: 2036017
-
Trehalose inhibits ethanol effects on intact yeast cells and liposomes.
Biochim Biophys Acta. 1994 May 11;1191(2):309-16
PMID: 8172916
-
Effect of cellular inositol content on ethanol tolerance of Saccharomyces cerevisiae in sake brewing.
J Biosci Bioeng. 2004;98(2):107-13
PMID: 16233674
-
Cloning genes by complementation in yeast.
Methods Enzymol. 1991;194:195-230
PMID: 2005788
-
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54
PMID: 942051
-
Proline biosynthesis in Saccharomyces cerevisiae: analysis of the PRO3 gene, which encodes delta 1-pyrroline-5-carboxylate reductase.
J Bacteriol. 1992 Jun;174(11):3782-8
PMID: 1592829
-
Unusual solution properties of proline and its interaction with proteins.
Biochim Biophys Acta. 1978 Jun 15;541(2):270-7
PMID: 667127
-
Overexpression of the OLE1 gene enhances ethanol fermentation by Saccharomyces cerevisiae.
Appl Microbiol Biotechnol. 2000 May;53(5):568-74
PMID: 10855717
-
Cloning and characterization of a gene complementing the mutation of an ethanol-sensitive mutant of sake yeast.
Biosci Biotechnol Biochem. 2000 Feb;64(2):229-36
PMID: 10737174