Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking

Yeasts are predominant in the ancient and complex process of winemaking. In spontaneous fermentations, there is a progressive growth pattern of indigenous yeasts, with the final stages invariably being dominated by the alcohol‐tolerant strains of Saccharomyces cerevisiae. This species is universally known as the ‘wine yeast’ and is widely preferred for initiating wine fermentations. The primary role of wine yeast is to catalyze the rapid, complete and efficient conversion of grape sugars to ethanol, carbon dioxide and other minor, but important, metabolites without the development of off‐flavours. However, due to the demanding nature of modern winemaking practices and sophisticated wine markets, there is an ever‐growing quest for specialized wine yeast strains possessing a wide range of optimized, improved or novel oenological properties. This review highlights the wealth of untapped indigenous yeasts with oenological potential, the complexity of wine yeasts' genetic features and the genetic techniques often used in strain development. The current status of genetically improved wine yeasts and potential targets for further strain development are outlined. In light of the limited knowledge of industrial wine yeasts' complex genomes and the daunting challenges to comply with strict statutory regulations and consumer demands regarding the future use of genetically modified strains, this review cautions against unrealistic expectations over the short term. However, the staggering potential advantages of improved wine yeasts to both the winemaker and consumer in the third millennium are pointed out. Copyright © 2000 John Wiley & Sons, Ltd.

[1]  B. Gump,et al.  Production wine analysis , 1995 .

[2]  A. Teunissen,et al.  The dominant flocculation genes of Saccharomyces cerevisiae constitute a new subtelomeric gene family , 1995, Yeast.

[3]  A. Martini,et al.  Saccharomyces Meyen ex Reess , 1998 .

[4]  H. Yoshimoto,et al.  Effect of aeration and unsaturated fatty acids on expression of the Saccharomyces cerevisiae alcohol acetyltransferase gene , 1997, Applied and environmental microbiology.

[5]  F. Radler,et al.  Possible Use of Nisin in Winemaking. I. Action of Nisin Against Lactic Acid Bacteria and Wine Yeasts in Solid and Liquid Media , 1990, American Journal of Enology and Viticulture.

[6]  W. V. van Zyl,et al.  Cloning and expression of the α–L-arabinofuranosidase gene (ABF2) of Aspergillus niger in Saccharomyces cerevisiae , 1996, Applied Microbiology and Biotechnology.

[7]  G. Reed,et al.  Brewer’s Yeast , 1991 .

[8]  A. Querol,et al.  Construction of a recombinant wine yeast strain expressing beta-(1,4)-endoglucanase and its use in microvinification processes , 1993, Applied and environmental microbiology.

[9]  G. Smit,et al.  Cause and control of flocculation in yeast. , 1993, Trends in biotechnology.

[10]  H. Yoshimoto,et al.  Acetate ester production by Saccharomyces cerevisiae lacking the ATF1 gene encoding the alcohol acetyltransferase , 1996 .

[11]  G. Reglero,et al.  The Influence of the Yeast and Type of Culture on the Volatile Composition of Wines Fermented Without Sulfur Dioxide , 1990, American Journal of Enology and Viticulture.

[12]  J. Laencina,et al.  Vinification Effects on Changes in Volatile Compounds of Wine , 1994 .

[13]  I. Pretorius,et al.  A K2 neutral Saccharomyces cerevisiae strain contains a variant K2 M genome , 1990, Yeast.

[14]  J. Salmon.  Enological Fermentation Kinetics of an Isogenic Ploidy Series Derived from an Industrial Saccharomyces cerevisiae Strain , 1997 .

[15]  G. Fleet.  The microbiology of alcoholic beverages , 1998 .

[16]  R. Boulton,et al.  Yeast and Biochemistry of Ethanol Fermentation , 1999 .

[17]  I. S. Pretorius,et al.  Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. Takahashi,et al.  Genetic engineering of a sake yeast producing no urea by successive disruption of arginase gene , 1991, Applied and environmental microbiology.

[19]  E. Aubertin.  [Brewer's yeast]. , 1951, Journal de medecine de Bordeaux et du Sud-Ouest.

[20]  J. Teixeira,et al.  Effect of cultural and nutritional conditions on the control of flocculation expression in Saccharomyces cerevisiae. , 1994, Canadian journal of microbiology.

[21]  P. Barré,et al.  Mixed Lactic Acid–Alcoholic Fermentation by Saccharomyes cerevisiae Expressing the Lactobacillus casei L(+)–LDH , 1994, Bio/Technology.

[22]  J. Smith.  The impact of genetic engineering on food and beverage fermentations , 1998 .

[23]  T. H. Lee,et al.  Practical Implications of Malolactic Fermentation: A Review , 1985, American Journal of Enology and Viticulture.

[24]  G. Fink,et al.  Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. , 1996, Genetics.

[25]  A. Martini.  Origin and domestication of the wine yeast Saccharomyces cerevisiae , 1993 .

[26]  O. Kobayashi,et al.  Molecular cloning and analysis of the dominant flocculation gene FLO8 from Saccharomyces cerevisiae. , 1996, Molecular & general genetics : MGG.

[27]  F. Radler.  Possible Use of Nisin in Winemaking. II. Experiments to Control Lactic Acid Bacteria in the Production of Wine , 1990, American Journal of Enology and Viticulture.

[28]  S. Assinder,et al.  Yeast flocculation: Flo1 and NewFlo phenotypes and receptor structure , 1991, Yeast.

[29]  A. Querol,et al.  The application of molecular techniques in wine microbiology , 1996 .

[30]  K. Kobayashi,et al.  Hyperglycosylation of hen egg white lysozyme in yeast. , 1993, The Journal of biological chemistry.

[31]  G. Heard.  Novel yeasts in winemaking: looking to the future , 1999 .

[32]  I. S. Pretorius,et al.  Pseudohyphal and Invasive Growth in Saccharomyces Cerevisiae , 2001 .

[33]  K. Smart,et al.  The importance of surface charge and hydrophobicity for the flocculation of chain-forming brewing yeast strains and resistance of these parameters to acid washing. , 1995, FEMS microbiology letters.

[34]  P. Henschke.  Yeasts-metabolism of nitrogen compounds , 1993 .

[35]  E. A. Crowell,et al.  Formation of Ethyl Carbamate Precursors During Grape Juice (Chardonnay) Fermentation. I. Addition of Amino Acids, Urea, and Ammonia: Effects of Fortification on Intracellular and Extracellular Precursors , 1988, American Journal of Enology and Viticulture.

[36]  W. V. van Zyl,et al.  Co-expression of a Phanerochaete chrysosporium cellobiohydrolase gene and a Butyrivibrio fibrisolvens endo-β-1,4-glucanase gene in Saccharomyces cerevisiae , 1996, Current Genetics.

[37]  S. Keränen,et al.  CONSTRUCTION OF FLOCCULENT BREWER'S YEAST BY CHROMOSOMAL INTEGRATION OF THE YEAST FLOCCULATION GENE FLO1 , 1994 .

[38]  P. Barré,et al.  Acidification of Grape Musts by Saccharomyces cerevisiae Wine Yeast Strains Genetically Engineered to Produce Lactic Acid , 1999, American Journal of Enology and Viticulture.

[39]  J. Thevelein.  Regulation of Trehalose Metabolism and Its Relevance to cell Growth and Function , 1996 .

[40]  J. A. Barnett.  A history of research on yeasts 1: Work by chemists and biologists 1789–1850 , 1998, Yeast.

[41]  I. S. Pretorius,et al.  Engineering yeast for efficient cellulose degradation , 1998, Yeast.

[42]  R. Kunkee,et al.  Ester Concentration Differences in Wine Fermented by Various Species and Strains of Yeasts , 1982, American Journal of Enology and Viticulture.

[43]  P. Barré,et al.  Metabolic analysis of S. cerevisiae strains engineered for malolactic fermentation , 1997, FEBS letters.

[44]  P. Barré,et al.  Improvement of Nitrogen Assimilation and Fermentation Kinetics under Enological Conditions by Derepression of Alternative Nitrogen-Assimilatory Pathways in an Industrial Saccharomyces cerevisiae Strain , 1998, Applied and Environmental Microbiology.

[45]  P. Barré,et al.  Cloning, sequence and expression of the gene encoding the malolactic enzyme from Lactococcus lactis , 1993, FEBS letters.

[46]  C. G. Edwards,et al.  Production of Decanoic Acid and Other Volatile Compounds and the Growth of Yeast and Malolactic Bacteria During Vinification , 1990, American Journal of Enology and Viticulture.

[47]  A. Noble,et al.  Flavor chemistry and assessment , 1995 .

[48]  A. Iwamatsu,et al.  Molecular cloning, sequence analysis, and expression of the yeast alcohol acetyltransferase gene , 1994, Applied and environmental microbiology.

[49]  P. Barré,et al.  Stationary‐Phase Gene Expression in Saccharomyces cerevisiae During Wine Fermentation , 1997, Yeast.

[50]  E. Hinchliffe,et al.  Effect of Physiological Stress on the Surface Properties of Brewing Yeasts , 1995 .

[51]  L. Nykänen.  Formation and Occurrence of Flavor Compounds in Wine and Distilled Alcoholic Beverages , 1986, American Journal of Enology and Viticulture.

[52]  W. H. Zyl,et al.  Over-expression of the Saccharomyces cerevisiae exo-β-1,3-glucanase gene together with the Bacillus subtilis endo-β-1,3-1,4-glucanase gene and the Butyrivibrio fibrisolvens endo-β-1,4-glucanase gene in yeast , 1997 .

[53]  D. Stevens,et al.  Amino Acid Uptake by Four Commercial Yeasts at Two Different Temperatures of Growth and Fermentation: Effects on Urea Excretion and Reabsorption , 1991, American Journal of Enology and Viticulture.

[54]  Jeffrey W. Roberts,et al.  遺伝子の分子生物学 = Molecular biology of the gene , 1970 .

[55]  M. Aigle,et al.  Detection of polygalacturonase, pectin‐lyase and pectin‐esterase activities in a Saccharomyces cerevisiae strain , 1994, Yeast.

[56]  F. Zimmermann,et al.  Overproduction of glycolytic enzymes in yeast , 1989, Yeast.

[57]  I. Pretorius,et al.  MSS11, a novel yeast gene involved in the regulation of starch metabolism , 1997, Current Genetics.

[58]  P. Langridge,et al.  Validation of Bismuth-Containing Indicator Media for Predicting H2S-Producing Potential ofSaccharomyces cerevisiaeWine Yeasts Under Enological Conditions , 1995, American Journal of Enology and Viticulture.

[59]  I. Pretorius,et al.  Size differentiation of M2 genomes among K2 killer yeasts , 1989 .

[60]  H. Ibrahim,et al.  Bactericidal action of lysozymes attached with various sizes of hydrophobic peptides to the C‐terminal using genetic modification , 1997, FEBS letters.

[61]  D. Tipper,et al.  Cell cycle studies on the mode of action of yeast K28 killer toxin. , 1996, Microbiology.

[62]  R. Snow,et al.  Cloning the Gene for the Malolactic Fermentation of Wine from Lactobacillus delbrueckii in Escherichia coli and Yeasts , 1984, Applied and environmental microbiology.

[63]  I. S. Pretorius,et al.  Coexpression of the Bacillus pumilusβ-xylosidase (xynB) gene with the Trichoderma reeseiβ-xylanase 2 (xyn2) gene in the yeast Saccharomyces cerevisiae , 2000, Applied Microbiology and Biotechnology.

[64]  M. Aigle,et al.  Functional expression in Saccharomyces cerevisiae of the Lactococcus lactis mleS gene encoding the malolactic enzyme. , 1995, FEMS microbiology letters.

[65]  R. Snow.  Genetic Improvement of Wine Yeast , 1983 .

[66]  P. Barré,et al.  Malolactic fermentation by engineered Saccharomyces cerevisiae as compared with engineered Schizosaccharomyces pombe , 1996, Yeast.

[67]  P. Langridge,et al.  Amino Acid and Ammonium Utilization by Saccharomyces cerevisiae Wine Yeasts From a Chemically Defined Medium , 1995 .

[68]  M. D. Fumi,et al.  Recent Applications of Biotechnology in Wine Production , 1994 .

[69]  M. Mota,et al.  Flocculation onset, growth phase, and genealogical age in Saccharomyces cerevisiae. , 1996, Canadian journal of microbiology.

[70]  Graeme M. Walker,et al.  Yeast Physiology and Biotechnology , 1998 .

[71]  I. Pretorius,et al.  Synthesis and secretion of an Erwinia chrysanthemi pectate lyase in Saccharomyces cerevisiae regulated by different combinations of bacterial and yeast promoter and signal sequences. , 1992, Gene.

[72]  J. F. Gallander.  Deacidification of Eastern Table Wines With Schizosaccharomyces Pombe , 1977, American Journal of Enology and Viticulture.

[73]  C. Ough,et al.  Urea Removal from Wine by an Acid Urease , 1988, American Journal of Enology and Viticulture.

[74]  J. Ingraham,et al.  The formation of higher aliphatic alcohols by mutant strains of Saccharomyces cerevisiae. , 1960, Archives of biochemistry and biophysics.

[75]  B. Zoecklein.  Wine Analysis and Production , 1995 .

[76]  R. Young,et al.  Engineering pathways for malate degradation in Saccharomyces cerevisiae , 1997, Nature Biotechnology.

[77]  A. Tromp,et al.  Effect of Copperoxychloride on the Fermentation of Must and on Wine Quality , 2017 .

[78]  O. Kobayashi,et al.  Molecular cloning and analysis of the dominant flocculation gene , 1996 .

[79]  J. Adler-Nissen,et al.  Antimicrobial enzymes: Applications and future potential in the food industry , 1995 .

[80]  I. Pretorius,et al.  K3 killer yeast is a mutant K2 killer yeast , 1990 .

[81]  C. Kurtzman,et al.  Chapter 1 – Definition, Classification and Nomenclature of the Yeasts , 1998 .

[82]  R. Mortimer,et al.  Genome renewal: A new phenomenon revealed from a genetic study of 43 strains of Saccharomyces cerevisiae derived from natural fermentation of grape musts , 1994, Yeast.

[83]  D. Ellis,et al.  The Yeasts , 1921, Nature.

[84]  I. S. Pretorius,et al.  Effect of Increased Yeast Alcohol Acetyltransferase Activity on Flavor Profiles of Wine and Distillates , 2000, Applied and Environmental Microbiology.

[85]  M. J. Waites,et al.  NISIN AND BREWING , 1988 .

[86]  S. Avery,et al.  Copper toxicity towards Saccharomyces cerevisiae: dependence on plasma membrane fatty acid composition , 1996, Applied and environmental microbiology.

[87]  W. Hammes,et al.  New aspects for the application of nisin to food products based on its mode of action , 1986 .

[88]  L. Alberghina,et al.  Development of Metabolically Engineered Saccharomyces cerevisiae Cells for the Production of Lactic Acid , 1995, Biotechnology progress.

[89]  P. Langridge,et al.  Regulation of hydrogen sulfide liberation in wine-producing Saccharomyces cerevisiae strains by assimilable nitrogen , 1995, Applied and environmental microbiology.

[90]  A. Kato,et al.  Bactericidal action of lysozyme against gram-negative bacteria due to insertion of a hydrophobic pentapeptide into its C-terminus. , 1992, Bioscience, biotechnology, and biochemistry.

[91]  W. V. van Zyl,et al.  Expression of a Trichoderma reesei beta-xylanase gene (XYN2) in Saccharomyces cerevisiae , 1996, Applied and environmental microbiology.

[92]  Adelheid Stöckheim.  J. Lodder (Editor), The Yeasts. A Taxonomic Study. II. überarbeitete Auflage. X und 1385 S., 354 Abb. Amsterdam‐London 1970: North Holland Publ. Co. $ 65 , 1972 .

[93]  T. Herraiz,et al.  Formation of Ethyl Esters of Amino Acids by Yeasts During the Alcoholic Fermentation of Grape Juice , 1993, American Journal of Enology and Viticulture.

[94]  T. Shibamoto,et al.  Monitoring volatile chemicals formed from must during yeast fermentation , 1992 .

[95]  M. Takagi,et al.  Breeding of flocculent industrial alcohol yeast strains by self-cloning of the flocculation gene FLO1 and repeated-batch fermentation by transformants. , 1998, The Journal of general and applied microbiology.

[96]  C. Ough,et al.  Urea Excretion and Uptake by Wine Yeasts as Affected by Various Factors , 1993, American Journal of Enology and Viticulture.

[97]  P. Langridge,et al.  PCR differentiation of commercial yeast strains using intron splice site primers , 1996, Applied and environmental microbiology.

[98]  E. A. Crowell,et al.  Carbamyl Compound Reactions with Ethanol , 1988, American Journal of Enology and Viticulture.

[99]  I. Pretorius,et al.  A note on the primary structure and expression of an Erwinia carotovora polygalacturonase-encoding gene (peh1) in Escherichia coli and Saccharomyces cerevisiae. , 1993, The Journal of applied bacteriology.

[100]  J. D. de Winde,et al.  Novel sensing mechanisms and targets for the cAMP–protein kinase A pathway in the yeast Saccharomyces cerevisiae , 1999, Molecular microbiology.

[101]  M. Lachance,et al.  Ecology and yeasts , 1998 .

[102]  Gerald R. Fink,et al.  Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS , 1992, Cell.

[103]  P. Barré,et al.  Glycerol Overproduction by Engineered Saccharomyces cerevisiae Wine Yeast Strains Leads to Substantial Changes in By-Product Formation and to a Stimulation of Fermentation Rate in Stationary Phase , 1999, Applied and Environmental Microbiology.

[104]  J. Visser,et al.  Molecular cloning and expression in Saccharomyces cerevisiae of two Aspergillus nidulans xylanase genes , 1996, Applied and environmental microbiology.

[105]  P. Barré,et al.  Modulation of Glycerol and Ethanol Yields During Alcoholic Fermentation in Saccharomyces cerevisiae Strains Overexpressed or Disrupted for GPD1 Encoding Glycerol 3‐Phosphate Dehydrogenase , 1997, Yeast.

[106]  I. S. Pretorius,et al.  The development of bactericidal yeast strains by expressing the Pediococcus acidilactici pediocin gene (pedA) in Saccharomyces cerevisiae , 1999, Yeast.

[107]  J. Verbakel,et al.  Expression and secretion of antifreeze peptides in the yeast Saccharomyces cerevisiae , 1995, Yeast.

[108]  P. Langridge,et al.  The Escherichia coli ß-Glucuronidase Gene as a Marker for Saccharomyces Yeast Strain Identification , 1991 .

[109]  P. Romano,et al.  A biometric study of higher alcohol production in Saccharomyces cerevisiae. , 1990, Canadian journal of microbiology.

[110]  J. Ingraham,et al.  The pathway of formation of n-butyl and n-amyl alcohols by a mutant strain of Saccharomyces cerevisiae , 1961 .

[111]  C. Labarre,et al.  Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos , 1996, Applied and environmental microbiology.

[112]  R. Wickner,et al.  Double-stranded RNA viruses of Saccharomyces cerevisiae , 1996, Microbiological reviews.

[113]  R. Thornton.  The mapping of two dominant genes for foaming in wine yeasts , 1978 .

[114]  F. Berg,et al.  Flavour of distilled beverages , 1994 .

[115]  G. Fleet,et al.  Degradation of malic and tartaric acids by high density cell suspensions of wine yeasts , 1995 .

[116]  R. Wickner.  Killer yeasts. , 1985, Current topics in medical mycology.

[117]  P. Barré,et al.  Multiple Ty-mediated chromosomal translocations lead to karyotype changes in a wine strain of Saccharomyces cerevisiae , 1999, Molecular and General Genetics MGG.

[118]  P. Langridge,et al.  AFLP fingerprinting for analysis of yeast genetic variation. , 1999, International journal of systematic bacteriology.

[119]  W. Lo,et al.  FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin , 1996, Journal of bacteriology.

[120]  J. Poindexter,et al.  Combined procedure for assays of poly-β-hyroxybutyric acid and inorganic polyphosphate , 1983 .

[121]  I. S. Pretorius,et al.  Divergent Regulation of the Evolutionarily Closely Related Promoters of the Saccharomyces cerevisiae STA2 andMUC1 Genes , 1999, Journal of bacteriology.

[122]  C. Boone,et al.  Integration of the yeast K1 killer toxin gene into the genome of marked wine yeasts and its effect on vinification , 1990 .

[123]  I. S. Pretorius,et al.  Msn1p/Mss10p, Mss11p and Muc1p/Flo11p are part of a signal transduction pathway downstream of Mep2p regulating invasive growth and pseudohyphal differentiation in Saccharomyces cerevisiae , 1999, Molecular microbiology.

[124]  I. S. Pretorius,et al.  Coregulation of starch degradation and dimorphism in the yeast Saccharomyces cerevisiae. , 1997, Critical reviews in biochemistry and molecular biology.

[125]  P. Malcorps,et al.  A new model for the regulation of ester synthesis by alcohol acetyltransferase in saccharomyces cerevisiae during fermentation , 1991 .

[126]  M. Doyle,et al.  Behavior of Listeria monocytogenes in wiener exudates in the presence of Pediococcus acidilactici H or pediocin AcH during storage at 4 or 25 degrees C , 1991, Applied and environmental microbiology.

[127]  I. S. Pretorius,et al.  Cloning of the Bacillus pumilusβ-xylosidase gene (xynB ) and its expression in Saccharomyces cerevisiae , 1997, Applied Microbiology and Biotechnology.