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Sugar Metabolism by Saccharomyces and non-Saccharomyces Yeasts

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Biology of Microorganisms on Grapes, in Must and in Wine

This chapter summarizes the biochemistry and genetics of yeast carbohydrate metabolism. It mainly concentrates on data obtained for Saccharomyces cerevisiae and refers to other wine yeast only as far as important differences are concerned. The final part of this review describes the regulatory molecular mechanisms which govern glucose utilization.

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References

  • Afting EG, Ruppert D, Holzer H (1972) Yeast phosphofructokinase. II. Dependence of the ATP desensitization on effectors. Arch Biochem Biophys 152:433–439

    Article  PubMed  CAS  Google Scholar 

  • Aguilera A (1986) Deletion of the phosphoglucose isomerase structural gene makes growth and sporulation glucose dependent inSaccharomyces cerevisiae. Mol Gen Genet 204:310–316

    Article  PubMed  CAS  Google Scholar 

  • Arvanitidis A, Heinisch JJ (1994) Studies on the function of yeast phosphofructokinase subunits byin vitro mutagenesis. J Biol Chem 269: 8911–8918

    PubMed  CAS  Google Scholar 

  • Barnett JA (2003) Beginnings of microbiology and biochemistry: the contribution of yeast research. Microbiology 149:557–567

    Article  PubMed  CAS  Google Scholar 

  • Barnett JA, Payne RW, Yarrow D (2000) Yeasts: characteristics and identification. 3rd ed.,Cambridge University Press, Cambridge

    Google Scholar 

  • Bauer FF, Pretorius IS (2000) Yeast stress response and fermentation efficiency: how to survive the making of wine. S Afr J Enol Vitic 21:27–51

    CAS  Google Scholar 

  • Berthels NJ, Cordero Otero RR, Bauer FF, Pretorius IS, Thevelein JM (2008) Correlation between glucose/fructose discrepancy and hexokinase kinetic properties in differentSaccharomyces cerevisiae wine yeast strains. Appl Microbiol Biotechnol 77:1083–1091

    Article  PubMed  CAS  Google Scholar 

  • Berthels NJ, Cordero Otero RR, Bauer FF, Thevelein JM, Pretorius IS (2004) Discrepancy in glucose and fructose utilisation during fermentation bySaccharomyces cerevisiae wine yeast strains. FEMS Yeast Res 7:683–689

    Article  CAS  Google Scholar 

  • Bisson LF (1999) Stuck and sluggish fermentations. Am J Enol Vitic 50:107–119

    CAS  Google Scholar 

  • Bisson LF, Fraenkel DG (1983) Involvement of kinases in glucose and fructose uptake bySaccharomyces cerevisiae. Proc Natl Acad Sci U S A 80:1730–1734

    Article  PubMed  CAS  Google Scholar 

  • Boles E, Hollenberg CP (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21:85–111

    Article  PubMed  CAS  Google Scholar 

  • Boulton RB, Singleton VL, Bisson LF, Kunkee RE (1999) Yeast and biochemistry of ethanol fermentation. In: Principles and practices of winemaking. Springer Science + Buisness Media Inc., USA. Chapter 4:102–192

    Google Scholar 

  • Breunig KD, Bolotin-Fukuhara M, Bianchi MM, Bourgarel D, Falcone C, Ferrero I, Frontali L,Goffrini P, Krijger JJ, Mazzoni C, Milkowski C, Steensma H Y, Wesolowski-Louvel M,Zeeman AM (2000) Regulation of primary carbon metabolism inKluyveromyces lactis.Enzyme Microb Technol 26:771–780

    Article  PubMed  CAS  Google Scholar 

  • Chambers A (1997) Phosphoglycerate kinase. In: Zimmermann FK, Entian KD (eds) Yeast Sugar Metabolism. Technomic, Lancaster, PA, pp 141–156

    Google Scholar 

  • Ciani M, Ferraro L, Fatichenti F (2000) Influence of glycerol production on the aerobic and anaerobic growth of the wine yeastCandida stellata. Enzyme Microb Technol 27:698–703

    Article  PubMed  CAS  Google Scholar 

  • Ciriacy M (1975) Genetics of alcohol dehydrogenase inSaccharomyces cerevisiae. II. Two loci controlling synthesis of the glucose-repressible ADH II. Mol Gen Genet 138:157–164

    Article  PubMed  CAS  Google Scholar 

  • Cohen R, Yokoi T, Holland JP, Pepper AE, Holland MJ (1987) Transcription of the constitutively expressed yeast enolase geneENO1 is mediated by positive and negative cis-acting regulatory sequences. Mol Cell Biol 7:2753–2761

    PubMed  CAS  Google Scholar 

  • Compagno C, Boschi F, Ranzi BM (1996) Glycerol production in a triose phosphate isomerase deficient mutant ofSaccharomyces cerevisiae. Biotechnol Prog 12:591–595

    Article  PubMed  CAS  Google Scholar 

  • Dickinson JR (1999) Carbon metabolism. In: Dickinson JR, Schweizer M (eds) The Metabolism and Molecular Physiology ofSaccharomyces cerevisiae, Taylor and Francis, London, pp 23–55

    Google Scholar 

  • Entian KD, Barnett JA (1992) Regulation of sugar utilization bySaccharomyces cerevisiae.Trends Biochem Sci 17:506–510

    Article  PubMed  CAS  Google Scholar 

  • Ernandes JR, De Meirsman C, Rolland F, Winderickx J, de Winde J, Brandão RL, Thevelein JM (1998) During the initiation of fermentation overexpression of hexokinase PII in yeast transiently causes a similar deregulation of glycolysis as deletion oftps1. Yeast 14:255–269

    Article  PubMed  CAS  Google Scholar 

  • Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R, Kielland-Brandt MC, Lucas C, Brandt A (2005) A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter inSaccharomyces cerevisiae. Mol Biol Cell 16:2068–2076

    Article  PubMed  CAS  Google Scholar 

  • Fleet GH (1998) The microbiology of alcoholic beverages. In: Wood BJB (ed) Microbiology of Fermented Foods, Blackie, Glasgow, pp 217–262

    Google Scholar 

  • Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86:11–22

    Article  PubMed  CAS  Google Scholar 

  • Flores CL, Martínez-Costa OH, Sánchez V, Gancedo C, Aragón JJ (2005) The dimorphic yeastYarrowia lipolytica possesses an atypical phosphofructokinase: characterization of the enzyme and its encoding gene. Microbiology 151:1465–1474

    Article  PubMed  CAS  Google Scholar 

  • Flores CL, Rodriguez C, Petit T, Gancedo C (2000) Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev 24:507–529

    PubMed  CAS  Google Scholar 

  • Fraenkel DG (1982) Carbohydrate metabolism. In: Strathern JN, Jones EW, Broach JR (eds) The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression, Cold Spring Harbor Laboratory, New York, pp 1–37

    Google Scholar 

  • Francois J, Parrou JL (2001) Reserve carbohydrates metabolism in the yeastSaccharomyces cere-visiae. FEMS Microbiol Rev 25:125–145

    Article  PubMed  CAS  Google Scholar 

  • Fredlund E, Blank LM, Schnürer J, Sauer U, Passoth V (2004) Oxygen- and glucose-dependent regulation of central carbon metabolism inPichia anomala. Appl Environ Microbiol 70:5905–5911

    Article  PubMed  CAS  Google Scholar 

  • Gancedo C, Flores CL (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4:351–359

    Article  PubMed  CAS  Google Scholar 

  • Gancedo C, Serrano R (1989) Energy-yielding metabolism. In: Rose AH, Harrison JS (eds) The yeasts. Metabolism and Physiology of Yeasts, Academic, London, pp 205–259

    Google Scholar 

  • Gancedo JM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361

    PubMed  CAS  Google Scholar 

  • Gancedo JM, Gancedo C (1997) Gluconeogenesis and catabolite inactivation. In: Zimmermann FK, Entian KD (eds) Yeast Sugar Metabolism, Technomic, Lancaster, PA, pp 359–378

    Google Scholar 

  • Goffrini P, Wésolowski-Louvel M, Ferrero I (1991) A phosphoglucose isomerase gene is involved in the Rag phenotype of the yeastKluyveromyces lactis. Mol Gen Genet 228:401–409

    Article  PubMed  CAS  Google Scholar 

  • Golbik R, Naumann M, Otto A, Muller E, Behlke J, Reuter R, Hubner G, Kriegel TM (2001) Regulation of phosphotransferase activity of hexokinase 2 fromSaccharomyces cerevisiae by modification at serine-14. Biochemistry 40:1083–1090

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Siso MI, Freire-Picos MA, Ramil E, Gonzalez-Dominguez M, Rodriguez Torres A,Cerdan ME (2000) Respirofermentative metabolism inKluyveromyces lactis: Insights and perspectives. Enzyme Microb Technol 26:699–705

    Article  PubMed  CAS  Google Scholar 

  • Guillaume C, Delobel P, Sablayrolles JM, Blondin B (2007) Molecular basis of fructose utilization by the wine yeastSaccharomyces cerevisiae: a mutatedHXT3 allele enhances fructose fermentation. Appl Environ Microbiol 73:2432–2439

    Article  PubMed  CAS  Google Scholar 

  • Hedbacker K, Carlson M (2008) SNF1/AMPK pathways in yeast. Front Biosci 13:2408–2420

    Article  PubMed  CAS  Google Scholar 

  • Heinisch JJ, Rodicio R (1997) Fructose-1,6-bisphosphate aldolase, triosephosphate isomerase glyceraldehyde-3-phosphate dehydrogenases, and phosphoglycerate mutase. In: Zimmermann FK, Entian KD (eds) Yeast Sugar Metabolism, Technomic, Lancaster, PA, pp 119–140

    Google Scholar 

  • Heinisch JJ, Müller S, Schlüter E, Jacoby J, Rodicio R (1998) Investigation of two yeast genes encoding putative isoenzymes of phosphoglycerate mutase. Yeast 14:203–213

    Article  PubMed  CAS  Google Scholar 

  • Heinisch JJ, Boles E, Timpel C (1996) A yeast phosphofructokinase insensitive to the allosteric activator fructose 2,6-bisphosphate. Glycolysis/metabolic regulation/allosteric control. J Biol Chem 271:15928–15933

    Article  PubMed  CAS  Google Scholar 

  • Heinisch JJ, Hollenberg CP (1993) Yeasts. In: Rehm HJ, Reed G (eds) Biotechnology. VCH Verlagsgesellschaft mbH, Weinheim, pp 469–514

    Chapter  Google Scholar 

  • Henricsson C, de Jesus Ferreira MC, Hedfalk K, Elbing K, Larsson C, Bill RM, Norbeck J,Hohmann S, Gustafsson L (2005) Engineering of a novelSaccharomyces cerevisiae wine strain with a respiratory phenotype at high external glucose concentrations. Appl Environ Microbiol 71:6185–6192

    Article  PubMed  CAS  Google Scholar 

  • Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372

    Article  PubMed  CAS  Google Scholar 

  • Holsbeeks I, Lagatie O, Van Nuland A, Van de Velde S, Thevelein JM (2004) The eukaryotic plasma membrane as a nutrient-sensing device. Trends Biochem Sci 29:556–564

    Article  PubMed  CAS  Google Scholar 

  • Jacoby J, Hollenberg CP, Heinisch JJ (1993) Transaldolase mutants in the yeastKluyveromyces lactis provide evidence that glucose can be metabolized through the pentose phosphate pathway. Mol Microbiol 10:867–876

    Article  PubMed  CAS  Google Scholar 

  • Johnston M, Kim JH (2005) Glucose as a hormone: receptor-mediated glucose sensing in the yeastSaccharomyces cerevisiae. Biochem Soc Trans 33:247–252

    Article  PubMed  CAS  Google Scholar 

  • Kopperschläger G, Heinisch J (1997) Phosphofructokinase. In: Zimmermann FK, Entian KD (eds) Yeast Sugar Metabolism, Technomic, Lancaster, PA, pp 97–118

    Google Scholar 

  • Lagunas R (1981) IsSaccharomyces cerevisiae a typical facultative anaerobe? Trends Biochem Sci 6:201–202

    Article  CAS  Google Scholar 

  • Lagunas R (1993) Sugar transport inSaccharomyces cerevisiae. FEMS Microbiol Rev 10:229–242

    PubMed  CAS  Google Scholar 

  • Lilly M, Bauer FF, Lambrechts MG, Swiegers JH, Cozzolino D, Pretorius IS (2006) The effect of increased yeast alcohol acetyltransferase and esterase activity on the flavour profiles of wine and distillates. Yeast 23:641–659

    Article  PubMed  CAS  Google Scholar 

  • Luyten K, Riou C, Blondin B (2002) The hexose transporters ofSaccharomyces cerevisiae play different roles during enological fermentation. Yeast 19:713–726

    Article  PubMed  CAS  Google Scholar 

  • Maier A, Völker B, Boles E, Fuhrmann GF (2002) Characterisation of glucose transport inSaccharomyces cerevisiae with plasma membrane vesicles (countertransport) and intact cells (initial uptake) with single Hxt1, Hxt2, Hxt3, Hxt4, Hxt6, Hxt7 or Gal2 transporters. FEMS Yeast Res 2:539–550

    PubMed  CAS  Google Scholar 

  • McAlister L, Holland MJ (1985a) Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15013–15018

    CAS  Google Scholar 

  • McAlister L, Holland MJ (1985b) Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15019–15027

    CAS  Google Scholar 

  • Moreno F, Ahuatzi D, Riera A, Palomino CA, Herrero P (2005) Glucose sensing through the Hxk2-dependent signalling pathway. Biochem Soc Trans 33:265–268

    Article  PubMed  CAS  Google Scholar 

  • Morris CN, Ainsworth S, Kinderlerer J (1986) The regulatory properties of yeast pyruvate kinase.Effect of fructose 1,6-bisphosphate. Biochem J 234:691–698

    PubMed  CAS  Google Scholar 

  • Nissen P, Nielsen D, Arneborg N (2003) ViableSaccharomyces cerevisiae cells at high concentrations cause early growth arrest of non-Saccharomyces yeasts in mixed cultures by a cell-cell contact-mediated mechanism. Yeast 20:331–341

    Article  PubMed  CAS  Google Scholar 

  • Nourani A, Wesolowski-Louvel M, Delaveau T, Jacq C, Delahodde A (1997) Multiple-drug-resistance phenomenon in the yeastSaccharomyces cerevisiae: involvement of two hexose transporters. Mol Cell Biol 17:5453–5460

    PubMed  CAS  Google Scholar 

  • Özcan S, Johnston M (1999) Function and regulation of yeast hexose transporters. Microbiol Mol Biol Rev 63:554–569

    PubMed  Google Scholar 

  • Pearce AK, Crimmins K, Groussac E, Hewlins MJ, Dickinson JR, Francois J, Booth IR, Brown AJ (2001) Pyruvate kinase (Pyk1) levels influence both the rate and direction of carbon flux in yeast under fermentative conditions. Microbiology 147:391–401

    PubMed  CAS  Google Scholar 

  • Perez M, Luyten K, Michel R, Riou C, Blondin B (2005) Analysis ofSaccharomyces cerevisiaehexose carrier expression during wine fermentation: Both low- and high-affinity Hxt transporters are expressed. FEMS Yeast Res 5:351–361

    Article  PubMed  CAS  Google Scholar 

  • Portela P, Moreno S, Rossi S (2006) Characterization of yeast pyruvate kinase 1 as a protein kinase A substrate, and specificity of the phosphorylation site sequence in the whole protein.Biochem J 396:117–126

    Article  PubMed  CAS  Google Scholar 

  • Reifenberger E, Boles E, Ciriacy M (1997) Kinetic characterization of individual hexose transporters ofSaccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. Eur J Biochem 245:324–333

    Article  PubMed  CAS  Google Scholar 

  • Remize F, Andrieu E, Dequin S (2000) Engineering of the pyruvate dehydrogenase bypass inSaccharomyces cerevisiae: role of the cytosolic Mg(2+) and mitochondrial K(+) acetaldehyde dehydrogenases Ald6p and Ald4p in acetate formation during alcoholic fermentation. Appl Environ Microbiol 66:3151–3159

    Article  PubMed  CAS  Google Scholar 

  • Remize F, Roustan JL, Sablayrolles JM, Barre P, Dequin S (1999) Glycerol overproduction by engineeredSaccharomyces cerevisiae wine yeast strains leads to substantial changes in byproduct formation and to a stimulation of fermentation rate in stationary phase. Appl Environ Microbiol 65:143–149

    PubMed  CAS  Google Scholar 

  • Rodicio R, Heinisch JJ, Hollenberg CP (1993) Transcriptional control of yeast phosphoglycerate mutase-encoding gene. Gene 125:125–133

    Article  PubMed  CAS  Google Scholar 

  • Rodicio R, Strauss A, Heinisch JJ (2000) Single point mutations in either gene encoding the subunits of the heterooctameric yeast phosphofructokinase abolish allosteric inhibition by ATP. J Biol Chem 275:40952–40960

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Winderickx J, Thevelein JM (2002) Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2:183–201

    PubMed  CAS  Google Scholar 

  • Rossignol T, Dulau L, Julien A, Blondin B (2003) Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20:1369–1385

    Article  PubMed  CAS  Google Scholar 

  • Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jähn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS (1999) The major facilitator superfamily.J Mol Microbiol Biotechnol 1:257–279

    PubMed  CAS  Google Scholar 

  • Saint-Prix F, Bonquist L, Dequin S (2004) Functional analysis of theALD gene family ofSaccharomyces cerevisiae during anaerobic growth on glucose: The NADP+-dependent Ald6p and Ald5p isoforms play a major role in acetate formation. Microbiology 150:2209–2220

    Article  PubMed  CAS  Google Scholar 

  • Santangelo GM (2006) Glucose signaling inSaccharomyces cerevisiae. Microbiol Mol Biol Rev 70:253–282

    Article  PubMed  CAS  Google Scholar 

  • Schaaff I, Heinisch J, Zimmermann FK (1989) Overproduction of glycolytic enzymes in yeast.Yeast 5:285–290

    Article  PubMed  CAS  Google Scholar 

  • Schehl B, Müller C, Senn T, Heinisch JJ (2004) A laboratory yeast strain suitable for spirit production. Yeast 21:1375–1389

    Article  PubMed  CAS  Google Scholar 

  • Schmitt HD, Zimmermann FK (1982) Genetic analysis of the pyruvate decarboxylase reaction in yeast glycolysis. J Bacteriol 151:1146–1152

    PubMed  CAS  Google Scholar 

  • Schüller HJ (2003) Transcriptional control of nonfermentative metabolism in the yeastSaccharomyces cerevisiae. Curr Genet 43:139–160

    PubMed  Google Scholar 

  • Schwelberger HG, Kohlwein SD, Paltauf F (1989) Molecular cloning, primary structure and disruption of the structural gene of aldolase fromSaccharomyces cerevisiae. Eur J Biochem 180:301–308

    Article  PubMed  CAS  Google Scholar 

  • Tamás MJ, Karlgren S, Bill RM, Hedfalk K, Allegri L, Ferreira M, Thevelein JM, Rydstrom J,Mullins JG, Hohmann S (2003) A short regulatory domain restricts glycerol transport through yeast Fps1p. J Biol Chem 278:6337–6345

    Article  PubMed  Google Scholar 

  • Thevelein JM, Cauwenberg L, Colombo S, De Winde JH, Donation M, Dumortier F, Kraakman L, Lemaire K, Ma P, Nauwelaers D, Rolland F, Teunissen A, Van Dijck P, Versele M, Wera S,Winderickx J (2000) Nutrient-induced signal transduction through the protein kinase A pathway and its role in the control of metabolism, stress resistance, and growth in yeast. Enzyme Microb Technol 26:819–825

    Article  PubMed  CAS  Google Scholar 

  • Valadi H, Valadi A, Ansell R, Gustafsson L, Adler L, Norbeck J, Blomberg A (2004) NADH-reductive stress inSaccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1). Curr Genet 45:90–95

    Article  PubMed  CAS  Google Scholar 

  • Van Urk H, Voll WS, Scheffers WA, Van Dijken JP (1990) Transient-State Analysis of Metabolic Fluxes in Crabtree-Positive and Crabtree-Negative Yeasts. Appl Environ Microbiol 56:281–287

    PubMed  Google Scholar 

  • Verstrepen KJ, Iserentant D, Malcorps P, Derdelinckx G, Van Dijck P, Winderickx J, Pretorius IS,Thevelein JM, Delvaux FR (2004) Glucose and sucrose: Hazardous fast-food for industrial yeast?. Trends Biotechnol 22:531–537

    Article  PubMed  CAS  Google Scholar 

  • Verwaal R, Paalman JW, Hogenkamp A, Verkleij AJ, Verrips CT, Boonstra J (2002)HXT5 expression is determined by growth rates inSaccharomyces cerevisiae. Yeast 19:1029–1038

    Article  PubMed  CAS  Google Scholar 

  • Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses inSaccharomyces cerevisiae. FEBS Lett 464:123–128

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann FK, Entian KD (1997) Yeast sugar metabolism. Technomic, Lancaster, PA.

    Google Scholar 

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Rodicio, R., Heinisch, J.J. (2009). Sugar Metabolism by Saccharomyces and non-Saccharomyces Yeasts. In: König, H., Unden, G., Fröhlich, J. (eds) Biology of Microorganisms on Grapes, in Must and in Wine. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-85463-0_6

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