Yeast: the soul of beer’s aroma—a review of flavour-active esters and higher alcohols produced by the brewing yeast
Tóm tắt
Among the most important factors influencing beer quality is the presence of well-adjusted amounts of higher alcohols and esters. Thus, a heavy body of literature focuses on these substances and on the parameters influencing their production by the brewing yeast. Additionally, the complex metabolic pathways involved in their synthesis require special attention. More than a century of data, mainly in genetic and proteomic fields, has built up enough information to describe in detail each step in the pathway for the synthesis of higher alcohols and their esters, but there is still place for more. Higher alcohols are formed either by anabolism or catabolism (Ehrlich pathway) of amino acids. Esters are formed by enzymatic condensation of organic acids and alcohols. The current paper reviews the up-to-date knowledge in the pathways involving the synthesis of higher alcohols and esters by brewing yeasts. Fermentation parameters affecting yeast response during biosynthesis of these aromatic substances are also fully reviewed.
Tài liệu tham khảo
Alvarez P, Malcorps P, Almeida AS, Ferreira A, Meyer AM, Dufour JP (1994) Analysis of free fatty-acids, fusel alcohols, and esters in beer—an alternative to Cs2 extraction. J Am Soc Brew Chem 52:127–134
Anderson RG, Kirsop BH (1974) The control of volatile ester synthesis during the fermentation of wort of high specific gravity. J Inst Brew 80:48–55
Anderson RG, Kirsop BH (1975a) Oxygen as a regulator of ester accumulation during the fermentation of worts of high specific gravity. J Inst Brew 81:111–115
Anderson RG, Kirsop BH (1975b) Quantitative aspects of the control by oxygenation of acetate ester formation of worts of high specific gravity. J Inst Brew 81:269–301
Avalos JL, Fink GR, Stephanopoulos G (2013) Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat Biotechnol 31:335–341
Äyräptää T (1971) Biosynthetic formation of higher alcohols by yeast. Dependence on the nitrogen nutrient level of the medium. J Inst Brew 77:266–276
Baker CA, Morton S (1977) Oxygen levels in air-saturated worts. J Inst Brew 83:348–349
Bakker BM, Bro C, Kotter P, Luttik MA, van Dijken JP, Pronk JT (2000) The mitochondrial alcohol dehydrogenase Adh3p is involved in a redox shuttle in Saccharomyces cerevisiae. J Bacteriol 182:4730–4737
Bennetzen JL, Hall BD (1982) The primary structure of the Saccharomyces cerevisiae gene for alcohol dehydrogenase. J Biol Chem 257:3018–3025
Berner TS, Arneborg N (2012) The role of lager beer yeast in oxidative stability of model beer. Lett Appl Microbiol 54:225–232
Blasco L, Vinas M, Villa TG (2011) Proteins influencing foam formation in wine and beer: the role of yeast. Int Microbiol 14:61–71
Boer VM, Tai SL, Vuralhan Z, Arifin Y, Walsh MC, Piper MD, de Winde JH, Pronk JT, Daran JM (2007) Transcriptional responses of Saccharomyces cerevisiae to preferred and nonpreferred nitrogen sources in glucose-limited chemostat cultures. FEMS Yeast Res 7:604–620
Bolat I, Romagnoli G, Zhu F, Pronk JT, Daran JM (2013) Functional analysis and transcriptional regulation of two orthologs of ARO10, encoding broad-substrate-specificity 2-oxo-acid decarboxylases, in the brewing yeast Saccharomyces pastorianus CBS1483. FEMS Yeast Res 13:505–517
Branyik T, Silva DP, Baszczynski M, Lehnert R, Silva J (2012) A review of methods of low alcohol and alcohol-free beer production. J Food Eng 108:493–506
Bravi E, Perretti G, Buzzini P, Della Sera R, Fantozzi P (2009) Technological steps and yeast biomass as factors affecting the lipid content of beer during the brewing process. J Agric Food Chem 57:6279–6284
Buhligen F, Rudinger P, Fetzer I, Stahl F, Scheper T, Harms H, Muller S (2013) Sustainability of industrial yeast serial repitching practice studied by gene expression and correlation analysis. J Biotechnol 168:718–728
Calderbank J, Hammond JRM (1994) Influence of higher alcohol availability on ester formation by yeast. J Am Soc Brew Chem 52:84–90
Chen E-H (1978) Relative contribution of Ehrlich and biosynthetic pathways to the formation of fusel alcohols. J Am Soc Brew Chem 36:39–43
Cooper TG (2002) Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol Rev 26:223–238
Dekoninck T, Verbelen PJ, Delvaux F, Van Mulders SE, Delvaux F (2012) The importance of wort composition for yeast metabolism during accelerated brewery fermentations. J Am Soc Brew Chem 70:195–204
Dickinson JR, Norte V (1993) A study of branched-chain amino acid aminotransferase and isolation of mutations affecting the catabolism of branched-chain amino acids in Saccharomyces cerevisiae. FEBS Lett 326:29–32
Dickinson JR, Lanterman MM, Danner DJ, Pearson BM, Sanz P, Harrison SJ, Hewlins MJ (1997) A 13C nuclear magnetic resonance investigation of the metabolism of leucine to isoamyl alcohol in Saccharomyces cerevisiae. J Biol Chem 272:26871–26878
Dickinson JR, Harrison SJ, Hewlins MJ (1998) An investigation of the metabolism of valine to isobutyl alcohol in Saccharomyces cerevisiae. J Biol Chem 273:25751–25756
Dickinson JR, Harrison SJ, Dickinson JA, Hewlins MJ (2000) An investigation of the metabolism of isoleucine to active amyl alcohol in Saccharomyces cerevisiae. J Biol Chem 275:10937–10942
Dickinson JR, Salgado LE, Hewlins MJ (2003) The catabolism of amino acids to long chain and complex alcohols in Saccharomyces cerevisiae. J Biol Chem 278:8028–8034
Didion T, Grauslund M, Kielland-Brandt MC, Andersen HA (1996) Amino acids induce expression of BAP2, a branched-chain amino acid permease gene in Saccharomyces cerevisiae. J Bacteriol 178:2025–2029
Dufour JP (1994) Higher alcohols, acids and ester secretion during yeast growth. In: Proceedings of the 6th Jean De Clerck Chair. Academic, Leuven, pp 1–40
Eden A, Simchen G, Benvenisty N (1996) Two yeast homologs of ECA39, a target for c-Myc regulation, code for cytosolic and mitochondrial branched-chain amino acid aminotransferases. J Biol Chem 271:20242–20245
Eden A, Van Nedervelde L, Drukker M, Benvenisty N, Debourg A (2001) Involvement of branched-chain amino acid aminotransferases in the production of fusel alcohols during fermentation in yeast. Appl Microbiol Biotechnol 55:296–300
Ehrlich F (1907) Über die Bedingungen der Fuselölbildung und über ihren Zusammenhang mit dem Eiweissaufbau der Hefe. Ber Dtsch Chem Ges 40:1027–1047
Engan S (1970) Wort composition and beer flavour I: the influence of some amino acids on the formation of higher aliphatic alcohols and esters. J Inst Brew 76:254–261
Engan S (1974) Esters in beer. J Inst Brew Dig 49:40–48
Engan S (1981) Beer composition: volatile substances. In: Pollock JRA (ed) Brewing science, vol 2. Academic, London, pp 93–165
Engan S and Aubert O (1977) Relations between fermentation temperature and the formation of some flavour components. In: 16th European brewery convention congress, pp 591–607, Netherlands, Amsterdam
Fujii T, Nagasawa N, Iwamatsu A, Bogaki T, Tamai Y, Hamachi M (1994) Molecular cloning, sequence analysis, and expression of the yeast alcohol acetyltransferase gene. Appl Environ Microbiol 60:2786–2792
Fujii T, Yoshimoto H, Nagasawa N, Bogaki T, Tamai Y, Hamachi M (1996) Nucleotide sequences of alcohol acetyltransferase genes from lager brewing yeast, Saccharomyces carlsbergensis. Yeast 12:593–598
Fujii T, Kobayashi O, Yoshimoto H, Furukawa S, Tamai Y (1997) Effect of aeration and unsaturated fatty acids on expression of the Saccharomyces cerevisiae alcohol acetyltransferase gene. Appl Environ Microbiol 63:910–915
Fujiwara D, Yoshimoto H, Sone H, Harashima S, Tamai Y (1998) Transcriptional co-regulation of Saccharomyces cerevisiae alcohol acetyltransferase gene, ATF1 and delta-9 fatty acid desaturase gene, OLE1 by unsaturated fatty acids. Yeast 14:711–721
Fujiwara D, Kobayashi O, Yoshimoto H, Harashima S, Tamai Y (1999) Molecular mechanism of the multiple regulation of the Saccharomyces cerevisiae ATF1 gene encoding alcohol acetyltransferase. Yeast 15:1183–1197
Fukuda K, Kuwahata O, Kiyokawa Y, Yanagiuchi T, Wakai Y, Kitamoto K, Inoue Y, Kimura A (1996) Molecular cloning and nucleotide sequence of the isoamyl acetate-hydrolyzing esterase gene (EST2) from Saccharomyces cerevisiae. J Ferment Bioeng 82:8–15
Fukuda K, Yamamoto N, Kiyokawa Y, Yanagiuchi T, Wakai Y, Kitamoto K, Inoue Y, Kimura A (1998a) Balance of activities of alcohol acetyltransferase and esterase in Saccharomyces cerevisiae is important for production of isoamyl acetate. Appl Environ Microbiol 64:4076–4078
Fukuda K, Yamamoto N, Kiyokawa Y, Yanagiuchi T, Wakai Y, Kitamoto K, Inoue Y, Kimura A (1998b) Brewing properties of sake yeast whose EST2 gene encoding isoamyl acetate-hydrolyzing esterase was disrupted. J Ferment Bioeng 85:101–106
Gibson BR, Lawrence SJ, Boulton CA, Box WG, Graham NS, Linforth RS, Smart KA (2008) The oxidative stress response of a lager brewing yeast strain during industrial propagation and fermentation. FEMS Yeast Res 8:574–585
Hiralal L, Olaniran AO, Pillay B (2013) Aroma-active ester profile of ale beer produced under different fermentation and nutritional conditions. J Biosci Bioeng 117:57–64
Hofman-Bang J (1999) Nitrogen catabolite repression in Saccharomyces cerevisiae. Mol Biotechnol 12:35–73
Hull G (2008) Olive oil addition to yeast as an alternative to wort aeration. Technol Q Master Brew Assoc Am 45:17–23
Iraqui I, Vissers S, Andre B, Urrestarazu A (1999) Transcriptional induction by aromatic amino acids in Saccharomyces cerevisiae. Mol Cell Biol 19:3360–3371
Jenkins CL, Kennedy AI, Hodgson JA, Pa T, Smart KA (2003) Impact of serial repitching on lager brewing yeast quality. J Am Soc Brew Chem 61:1–9
Kispal G, Steiner H, Court DA, Rolinski B, Lill R (1996) Mitochondrial and cytosolic branched-chain amino acid transaminases from yeast, homologs of the myc oncogene-regulated Eca39 protein. J Biol Chem 271:24458–24464
Knatchbull FB, Slaughter JC (1987) The effect of low CO2 pressure on the absorption of amino acids and production of flavour-active volatiles by yeast. J Inst Brew 93:420–424
Kohlhaw GB (2003) Leucine biosynthesis in fungi: entering metabolism through the back door. Microbiol Mol Biol Rev 67:1–15, table of contents
Krogerus K, Gibson BR (2013) Diacetyl and its control during brewery fermentation. J Inst Brew 119:86–97
Landaud S, Latrille E, Corrieu G (2001) Top pressure and temperature control the fusel alcohol/ester ratio through yeast growth in beer fermentation. J Inst Brew 107:107–117
Lee K, Hahn JS (2013) Interplay of Aro80 and GATA activators in regulation of genes for catabolism of aromatic amino acids in Saccharomyces cerevisiae. Mol Microbiol 88:1120–1134
Lee K, Sung C, Kim BG, Hahn JS (2013) Activation of Aro80 transcription factor by heat-induced aromatic amino acid influx in Saccharomyces cerevisiae. Biochem Biophys Res Commun 438:43–47
Lei H, Zhao H, Yu Z, Zhao M (2012) Effects of wort gravity and nitrogen level on fermentation performance of brewer’s yeast and the formation of flavor volatiles. Appl Biochem Biotechnol 166:1562–1574
Lei H, Li H, Mo F, Zheng L, Zhao H, Zhao M (2013a) Effects of Lys and His supplementations on the regulation of nitrogen metabolism in lager yeast. Appl Microbiol Biotechnol 97:8913–8921
Lei H, Zhao H, Zhao M (2013b) Proteases supplementation to high gravity worts enhances fermentation performance of brewer’s yeast. Biochem Eng J 77:1–6
Lei H, Zheng L, Wang C, Zhao H, Zhao M (2013c) Effects of worts treated with proteases on the assimilation of free amino acids and fermentation performance of lager yeast. Int J Food Microbiol 161:76–83
Libkind D, Hittinger CT, Valerio E, Goncalves C, Dover J, Johnston M, Goncalves P, Sampaio JP (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A 108:14539–14544
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
Lodolo EJ, Kock JL, Axcell BC, Brooks M (2008) The yeast Saccharomyces cerevisiae—the main character in beer brewing. FEMS Yeast Res 8:1018–1036
Ma J, Lu Q, Yuan Y, Ge H, Li K, Zhao W, Gao Y, Niu L, Teng M (2011) Crystal structure of isoamyl acetate-hydrolyzing esterase from Saccharomyces cerevisiae reveals a novel active site architecture and the basis of substrate specificity. Proteins 79:662–668
Malcorps P, Dufour JP (1992) Short-chain and medium-chain aliphatic-ester synthesis in Saccharomyces cerevisiae. Eur J Biochem 210:1015–1022
Malcorps P, Cheval JM, Jamil S, Dufour J-P (1991) A new model for the regulation of ester synthesis by alcohol acetyltransferase in Saccharomyces cerevisiae. J Am Soc Brew Chem 49:47–53
Mason AB, Dufour JP (2000) Alcohol acetyltransferases and the significance of ester synthesis in yeast. Yeast 16:1287–1298
Meilgaard MC (1975a) Flavor chemistry of beer: part I: flavor interaction between principal volatiles. MBAA. Technol Q 12:107–117
Meilgaard MC (1975b) Flavour chemistry of beer. Part II: flavor and threshold of 239 aroma volatiles. MBAA. Technol Q 12:151–168
Meilgaard MC (1991) The flavor of beer. MBAA Technol Q 28:132–141
Mojzita D, Hohmann S (2006) Pdc2 coordinates expression of the THI regulon in the yeast Saccharomyces cerevisiae. Mol Genet Genomics 276:147–161
Molina AM, Swiegers JH, Varela C, Pretorius IS, Agosin E (2007) Influence of wine fermentation temperature on the synthesis of yeast-derived volatile aroma compounds. Appl Microbiol Biotechnol 77:675–687
Montanari L, Marconi O, Mayer H, Fantozzi P (2009) Production of alcohol-free beer. In: Beer in health and disease prevention. Elsevier, Burlington, pp 61–75
Moonjai N, Verstrepen KJ, Delvaux FR, Derdelinckx G, Verachtert H (2002) The effects if linoleic acid supplementation of cropped yeast on its subsequent fermentation performance and acetate ester synthesis. J Inst Brew 108:227–235
Nagasawa N, Bogaki T, Iwamatsu A, Hamachi M, Kumagai C (1998) Cloning and nucleotide sequence of the alcohol acetyltransferase II gene (ATF2) from Saccharomyces cerevisiae Kyokai No. 7. Biosci Biotechnol Biochem 62:1852–1857
Neubauer O, Fromherz K (1911) Über den Abbau der Aminosäuren bei der Hefegärung. Hoppe-Seyler’s Z. Physiol Chem 70:326–350
Neven H, Delvaux F, Derdelinckx G (1997) Flavor evolution of top fermented beers. MBAA Technol Q 34:115–118
Nordström K (1962) Formation of ethyl acetate in fermentation with brewer’s yeast III. Participation of coenzyme A. J Inst Brew 68:398–407
Nykanen L, Nykanen I (1977) Production of esters by different yeast strains in sugar fermentations. J Inst Brew 83:30–31
Nykanen I, Suomalainen H (1983) Formation of aroma compounds by yeast. In: Nyaken I, Suomalainen H (eds) Aroma of beer, wine and distilled beverages. Reidel, Dordrecht, pp 3–16
Nykiinen L, Nykiinen I, Suomalainen H (1977) Distribution of esters produced during sugar fermentation between the yeast cell and the medium. J Inst Brew 83:32–34
Oshita K, Kubota M, Uchida Ma, and Ono M (1995) Clarification of the relationship between fusel alcohol formation and amino acid assimilation by brewing yeast using 13C-labeled amino acid. In: 25th European brewery convention congress, pp 387–402, Brussels
Peddie HAB (1990) Ester formation in brewery fermentations. J Inst Brew Dig 96:327–331
Perpete P, Collin S (2000) Influence of beer ethanol content on the wort flavour perception. Food Chem 71:379–385
Picotti P, Clement-Ziza M, Lam H, Campbell DS, Schmidt A, Deutsch EW, Rost H, Sun Z, Rinner O, Reiter L, Shen Q, Michaelson JJ, Frei A, Alberti S, Kusebauch U, Wollscheid B, Moritz RL, Beyer A, Aebersold R (2013) A complete mass-spectrometric map of the yeast proteome applied to quantitative trait analysis. Nature 494:266–270
Piddocke MP, Kreisz S, Heldt-Hansen HP, Nielsen KF, Olsson L (2009) Physiological characterization of brewer’s yeast in high-gravity beer fermentations with glucose or maltose syrups as adjuncts. Appl Microbiol Biotechnol 84:453–464
Powell CD, Diacetis AN (2007) Long term serial repitching and the genetic and phenotypic stability of brewer’s yeast. J Inst Brew 113:67–74
Procopio S, Krausea D, Hofmannb T, Beckera T (2013) Significant amino acids in aroma compound profiling during yeast fermentation analyzed by PLS regression. LWT Food Sci Technol 51:423–432
Ramos-Jeunehomme C, Laub R, Masschelein CA (1991) Why is ester formation in brewery fermentations yeast strain dependent? In: 23rd European brewery convention congress. Oxford University, Lisbon, pp 257–264
Renger RS, Van Hateren SH, Luyben KCAM (1992) The formation of esters and higher alcohols during brewery fermentation—the effect of carbon dioxide pressure. J Inst Brew 98:509–513
Rice JF, Chicoye E, Helbert JR (1977) Inhibition ofbeer volatiles formation by carbon dioxide pressure. J Am Soc Brew Chem 35:35–40
Rodrigues JA, Barros AS, Carvalho B, Brandao T, Gil AM (2011) Probing beer aging chemistry by nuclear magnetic resonance and multivariate analysis. Anal Chim Acta 702:178–187
Romagnoli G, Luttik MA, Kotter P, Pronk JT, Daran JM (2012) Substrate specificity of thiamine pyrophosphate-dependent 2-oxo-acid decarboxylases in Saccharomyces cerevisiae. Appl Environ Microbiol 78:7538–7548
Rossouw D, Naes T, Bauer FF (2008) Linking gene regulation and the exo-metabolome: a comparative transcriptomics approach to identify genes that impact on the production of volatile aroma compounds in yeast. BMC Genomics 9:530
Russell DW, Smith M, Williamson VM, Young ET (1983) Nucleotide sequence of the yeast alcohol dehydrogenase II gene. J Biol Chem 258:2674–2682
Saerens SM, Verstrepen KJ, Van Laere SD, Voet AR, Van Dijck P, Delvaux FR, Thevelein JM (2006) The Saccharomyces cerevisiae EHT1 and EEB1 genes encode novel enzymes with medium-chain fatty acid ethyl ester synthesis and hydrolysis capacity. J Biol Chem 281:4446–4456
Saerens SM, Delvaux F, Verstrepen KJ, Van Dijck P, Thevelein JM, Delvaux FR (2008a) Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol 74:454–461
Saerens SM, Verbelen PJ, Vanbeneden N, Thevelein JM, Delvaux FR (2008b) Monitoring the influence of high-gravity brewing and fermentation temperature on flavour formation by analysis of gene expression levels in brewing yeast. Appl Microbiol Biotechnol 80:1039–1051
Saison D, De Schutter DP, Uyttenhove B, Delvaux F, Delvaux FR (2009) Contribution of staling compounds to the aged flavour of lager beer by studying their flavour thresholds. Food Chem 114:1206–1215
Sato M, Watari J, Ha S, Koshino S (1994) Instability in electrophoretic karyotype of brewing yeasts. J Am Soc Brew Chem 52:148–151
Schoondermark-Stolk SA, Tabernero M, Chapman J, Ter Schure EG, Verrips CT, Verkleij AJ, Boonstra J (2005) Bat2p is essential in Saccharomyces cerevisiae for fusel alcohol production on the non-fermentable carbon source ethanol. FEMS Yeast Res 5:757–766
Sentheshanmuganathan S, Elsden SR (1958) The mechanism of the formation of tyrosol by Saccharomyces cerevisiae. Biochem J 69:210–218
Sentheshanuganathan S (1960) The mechanism of the formation of higher alcohols from amino acids by Saccharomyces cerevisiae. Biochem J 74:568–576
Shanta Kumara HMC, Fukui N, Kojima K, Nakatani K (1995) Regulation mechanism of ester formation by dissolved carbon dioxide during beer fermentation. MBAA Technol Q 32:159–162
Shindo S, Murakani J, Koshino S (1992) Control of acetate ester formation during alcohol fermentation with immobilized yeast. J Ferment Bioeng 73:370–374
Stewart G (2007) High gravity brewing- the pros and cons. New Food 1:42–46
Strejc J, Siříšťová L, Karabín M, Silva J, Brányik T (2013) Production of alcohol-free beer with elevated amounts of flavouring compounds using lager yeast mutants. J Inst Brew 119:149–155
Suomalainen H (1981) Yeast esterases and aroma esters in alcoholic beverages. J Inst Brew 87:296–300
Taylor GT, Tburston PA, Kirsop BH (1979) lnfluence of lipids derived from malt spent grains on yeast metabolism and fermentation. J Inst Brew 85:219–227
Thurston PA, Quain DE, Tuhh RS (1982) Lipid metabolism and the regulation of volatile synthesis in Saccharomyces cerevisiae. J Inst Brew 88:90–94
Urrestarazu A, Vissers S, Iraqui I, Grenson M (1998) Phenylalanine- and tyrosine-auxotrophic mutants of Saccharomyces cerevisiae impaired in transamination. Mol Gen Genet 257:230–237
Vanderhaegen B, Neven H, Coghe S, Verstrepen KJ, Derdelinckx G, Verachtert H (2003) Bioflavoring and beer refermentation. Appl Microbiol Biotechnol 62:140–150
Vanderhaegen B, Neven H, Verachtert H, Derdelinckx G (2006) The chemistry of beer aging—a critical review. Food Chem 95:357–381
Vasconcelles MJ, Jiang Y, McDaid K, Gilooly L, Wretzel S, Porter DL, Martin CE, Goldberg MA (2001) Identification and characterization of a low oxygen response element involved in the hypoxic induction of a family of Saccharomyces cerevisiae genes. Implications for the conservation of oxygen sensing in eukaryotes. J Biol Chem 276:14374–14384
Vaughan MA, Kurtzman CP (1985) Deoxyribonucleic acid relatedness among species of the genus Saccharomyces sensu stricto. Int J Syst Bacteriol 35:508–511
Verbelen PJ, Dekoninck TM, Saerens SM, Van Mulders SE, Thevelein JM, Delvaux FR (2009) Impact of pitching rate on yeast fermentation performance and beer flavour. Appl Microbiol Biotechnol 82:155–167
Verstrepen KJ, Derdelinckx G, Dufour JP, Winderickx J, Pretorius IS, Thevelein JM, Delvaux FR (2003a) The Saccharomyces cerevisiae alcohol acetyl transferase gene ATF1 is a target of the cAMP/PKA and FGM nutrient-signalling pathways. FEMS Yeast Res 4:285–296
Verstrepen KJ, Van Laere SD, Vanderhaegen BM, Derdelinckx G, Dufour JP, Pretorius IS, Winderickx J, Thevelein JM, Delvaux FR (2003b) Expression levels of the yeast alcohol acetyltransferase genes ATF1, Lg-ATF1, and ATF2 control the formation of a broad range of volatile esters. Appl Environ Microbiol 69:5228–5237
Vieira E, Brandao T, Ferreira IM (2013) Evaluation of brewer’s spent yeast to produce flavor enhancer nucleotides: influence of serial repitching. J Agric Food Chem 61:8724–8729
Vuralhan Z, Morais MA, Tai SL, Piper MD, Pronk JT (2003) Identification and characterization of phenylpyruvate decarboxylase genes in Saccharomyces cerevisiae. Appl Environ Microbiol 69:4534–4541
Vuralhan Z, Luttik MA, Tai SL, Boer VM, Morais MA, Schipper D, Almering MJ, Kotter P, Dickinson JR, Daran JM, Pronk JT (2005) Physiological characterization of the ARO10-dependent, broad-substrate-specificity 2-oxo acid decarboxylase activity of Saccharomyces cerevisiae. Appl Environ Microbiol 71:3276–3284
Williams RS, Wagner HP (1978) The isolation and identification of new staling related compounds form beer. J Am Soc Brew Chem 36:27–31
Williams RS, Wagner HP (1979) Contribution of hop bitter substances to beer staling mechanisms. J Am Soc Brew Chem 37:13–19
Yoshimoto H, Fujiwara D, Momma T, Ito C, Sone H, Kaneko Y, Tamai Y (1998) Characterization of the ATF1 and Lg-ATF1 genes encoding alcohol acetyltransferases in the bottom fermenting yeast Saccharomyces pastorianus. J Ferment Bioeng 86:15–20
Yoshioka K, Hashimoto N (1981) Ester formation by alcohol acetyltransferase from brewers yeast. Agric Biol Chem 45:2183–2190
Younis OS, Stewart GG (1998) Sugar uptake and subsequent ester and higher alcohol production by Saccharomyces cerevisiae. J Inst Brew 104:255–264
Younis OS, Stewart GG (1999) The effect of malt wort, very high gravity malt wart and very high gravity adjunct wort on volatile production in Saccharomyces cerevisiae. J Am Soc Brew Chem 57:39–45
Younis OS, Stewart GG (2000) The effect of wort maltose content on volatile production and fermentation performance in brewing yeast. In: Smart K (ed) Brewing yeast fermentation performance, 1st edn. Blackwell, Oxford, pp 170–176
Yu Z, Zhao H, Li H, Zhang Q, Lei H, Zhao M (2012) Selection of Saccharomyces pastorianus variants with improved fermentation performance under very high gravity wort conditions. Biotechnol Lett 34:365–370
Yukiko K, Fumihiko O, Keiji M, Toshihiko A (2001) Control of higher alcohol production by manipulation of the BAP2 gene in brewing yeast. J Am Soc Brew Chem 59:157–162
Zhang C, Liu Y, Qi Y, Zhang J, Dai L, Lin X, Xiao D (2013) Increased esters and decreased higher alcohols production by engineered brewer’s yeast strains. Eur Food Res Technol 236:1009–1014