Production and biological function of volatile esters in Saccharomyces cerevisiae

Microbial Biotechnology

Volumn 3, Issue 2, 2010, Pages 165-177

  Saerens, Sofie M G ^a   Delvaux, Freddy R ^a   Verstrepen, Kevin J ^a   Thevelein, Johan M ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETIC ACID ETHYL ESTER; ACETYL COENZYME A; ACTIVATING TRANSCRIPTION FACTOR 1; ACTIVATING TRANSCRIPTION FACTOR 2; ACYLTRANSFERASE; ESTER; HEXANOIC ACID; ISOPENTYL ACETATE; MEDIUM CHAIN FATTY ACID; UNSATURATED FATTY ACID; VOLATILE AGENT;

ALLELE; BEER; BEVERAGE; BIOCHEMISTRY; BIOLOGY; CLONE; DETOXIFICATION; ENZYME ACTIVITY; FERMENTATION; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HYDROLYSIS; HYPOTHESIS; NONHUMAN; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SHORT SURVEY; SYNTHESIS; WINE; YEAST;

ALCOHOLIC BEVERAGES; ESTERS; SACCHAROMYCES CEREVISIAE; VOLATILE ORGANIC COMPOUNDS;

SACCHAROMYCES CEREVISIAE;

EID: 77953604488     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2009.00106.x     Document Type: Short Survey

References (81)

1. Anderson, R.G., and Kirsop, B.H. (1975) Oxygen as a regulator of ester accumulation during fermentation of wort of high specific gravity. J Inst Brew 81: 111-115.
2. Anderson, R.J., and Kirsop, B.H. (1974) The control of volatile ester synthesis during the fermentation of wort of high specific gravity. J Inst Brew 80: 48-55.
3. Aritomi, K., Hirosawa, I., Hoshida, H., Shiigi, M., Nishizawa, Y., Kashiwagi, S., and Akada, R. (2004) Self-cloning yeast strains containing novel FAS2 mutations produce a higher amount of ethyl caproate in Japanese sake. Biosci Biotechnol Biochem 68: 206-214.
4. Asahina, K., Pavlenkovich, V., and Vosshall, L.B. (2008) The survival advantage of olfaction in a competitive environment. Curr Biol 18: 1153-1155.
5. Asahina, K., Louis, M., Piccinotti, S., and Vosshall, L.B. (2009) A circuit supporting concentration-invariant odor perception in Drosophila. J Biol 8: 9.
6. Äyräpää, T., and Lindström, and I. (1977) Aspects of the influence of exogenous fatty acids on the fatty acid metabolism of yeast. Proc Eur Brew Conv 16: 507-517.
7. Bardi, L., Crivelli, C., and Marzona, M. (1998) Esterase activity and release of ethyl esters of medium-chain fatty acids by Saccharomyces cerevisiae during anaerobic growth. Can J Microbiol 44: 1171-1176.
8. Bardi, L., Cocito, C., and Marzona, M. (1999) Saccharomyces cerevisiae cell fatty acid composition and release during fermentation without aeration and in absence of exogenous lipids. Int J Food Microbiol 47: 133-140.
9. Carrau, F.M., Medina, K., Farina, L., Boido, E., Henschke, P.A., and Dellacassa, E. (2008) Production of fermentation aroma compounds by Saccharomyces cerevisiae wine yeasts: effects of yeast assimilable nitrogen on two model strains. FEMS Yeast Res 8: 1196-1207.
10. Cauet, G., Degryse, E., Ledoux, C., Spagnoli, R., and Achstetter, T. (1999) Pregnenolone esterification in Saccharomyces cerevisiae - a potential detoxification mechanism. Eur J Biochem 261: 317-324.
11. Chellappa, R., Kandasamy, P., Oh, C.S., Jiang, Y., Vemula, M., and Martin, C.E. (2001) The membrane proteins, Spt23p and Mga2p, play distinct roles in the activation of Saccharomyces cerevisiae OLE1 gene expression - fatty acid-mediated regulation of Mga2p activity is independent of its proteolytic processing into a soluble transcription activator. J Biol Chem 276: 43548-43556.
12. Cordente, A.G., Swiegers, J.H., Hegardt, F.G., and Pretorius, I.S. (2007) Modulating aroma compounds during wine fermentation by manipulating carnitine acetyltransferases in Saccharomyces cerevisiae. FEMS Microbiol Lett 267: 159-166.
13. Crauwels, M., Donaton, M.C.V., Pernambuco, M.B., Winderickx, J., deWinde, J.H., and Thevelein, J.M. (1997) The Sch9 protein kinase in the yeast Saccharomyces cerevisiae controls cAPK activity and is required for nitrogen activation of the fermentable-growth-medium-induced (FGM) pathway. Microbiol-UK 143: 2627-2637.
14. Cristiani, G., and Monnet, V. (2001) Food micro-organisms and aromatic ester synthesis. Sci Aliments 21: 211-230.
15. Debourg, A. (2000) Yeast flavour metabolites. Eur Brew Conv Monogr 28: 60-73.
16. Dufour, J.-P., and Malcorps, P. (1994) Ester synthesis during fermentation: enzymes characterization and modulation mechanism. In Proceedings of the 4th Aviemore Conference on Malting, Brewing and Distilling. Campbell, I., and Priest, F. G. (eds). London, UK: The Institute of Brewing, pp. 137-151.
17. Dufour, J.-P., Verstrepen, K.J., and Derdelinckx, G. (2002) Brewing yeasts. In Yeasts in Food. Boekhout, T., and Robert, V. (eds). Hamburg, Germany: Behr's Verlag Gmbh & Co, pp. 347-388.
18. Dufour, J.-P., Malcorps, P., and Silcock, P. (2003) Control of ester synthesis during brewery fermentation. In Brewing Yeast Fermentation Performance. Smart, K. (ed.). Oxford, UK: Blackwell Publishing, pp. 213-233.
19. Fogleman, J.C., Starmer, W.T., and Heed, W.B. (1981) Larval selectivity for yeast species by Drosophila mojavensis in natural substrates. Proc Natl Acad Sci 78: 4435-4439.
20. Fujii, T., Nagasawa, N., Iwamatsu, A., Bogaki, T., Tamai, W., and Hamachi, M. (1994) Molecular cloning, sequence analysis, and expression of the yeast alcohol acetyltransferase gene. Appl Environ Microbiol 60: 2786-2792.
21. Fujii, T., Yoshimoto, H., Nagasawa, N., Bogaki, T., Tamai, Y., and Hamachi, M. (1996a) Nucleotide sequences of alcohol acetyltransferase genes from lager brewing yeast, Saccharomyces carlsbergensis. Yeast 12: 593-598.
22. Fujii, T., Yoshimoto, H., and Tamai, Y. (1996b) Acetate ester production by Saccharomyces cerevisiae lacking the ATF1 gene encoding the alcohol acetyltransferase. J Ferment Bioeng 81: 538-542.
23. Fujii, T., Kobayashi, O., Yoshimoto, H., Furukawa, S., and 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.
24. Fujiwara, D., Yoshimoto, H., Sone, H., Harashima, S., and 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.
25. Fujiwara, D., Kobayashi, O., Yoshimoto, H., Harashima, S., and Tamai, Y. (1999) Molecular mechanism of the multiple regulation of the Saccharomyces cerevisiae ATF1 gene encoding alcohol acetyltransferase. Yeast 15: 1183-1197.
26. Fukuda, K., Yamamoto, N., Kiyokawa, Y., Yanagiuchi, T., Wakai, Y., Kitamoto, K., et al. (1998) Balance of activities of alcohol acetyltransferase and esterase in Saccharomyces cerevisiae is important for production of isoamyl acetate. Appl Environ Microbiol 64: 4076-4078.
27. Furukawa, K, Yamada, T., Mizoguchi, H., and Hana, S. (2003) Increased ethyl caproate production by inositol limitation in Saccharomyces cerevisiae. J Biosci Bioeng 95: 448-454.
28. Haines, T.H. (2001) Do sterols reduce proton and sodium leaks through lipid bilayers?. Prog Lipid Res 40: 299-324.
29. Holmquist, M. (2000) Alpha/Beta-hydrolase fold enzymes: structures, functions and mechanisms. Curr Prot Pep Sci 1: 209-235.
30. Hunkova, Z., and Fencl, Z. (1977) Toxic effects of fatty acids on yeast cells - dependence of inhibitory effects on fatty acid concentration. Biotechnol Bioeng 19: 1623-1641.
31. Jiang, Y.D., Vasconcelles, M.J., Wretzel, S., Light, A., Martin, C.E., and Goldberg, M.A. (2001) MGA2 is involved in the low-oxygen response element-dependent hypoxic induction of genes in Saccharomyces cerevisiae. Mol Cell Biol 21: 6161-6169.
32. Kispal, G., Sumegi, B., Dietmeier, K., Bock, I., Gajdos, G., Tomcsanyi, T., and Sandor, A. (1993) Cloning and sequencing of a cDNA encoding Saccharomyces cerevisiae carnitine acetyltransferase - use of the cDNA in gene disruption studies. J Biol Chem 268: 1824-1829.
33. Li, Y.S., Zhao, Y.F., Hatfield, S., Wan, R., Zhu, Q., Li, X.H., et al. (2000) Dipeptide seryl-histidine and related oligopeptides cleave DNA, protein, and a carboxyl ester. Bioorgan Med Chem 8: 2675-2680.
34. Light, R.J., Lennarz, W.J., and Bloch, K. (1962) The metabolism of hydroxy stearic acids in yeast. J Biol Chem 237: 1793-1800.
35. Lilly, M., Lambrechts, M.G., and Pretorius, I.S. (2000) Effect of increased yeast alcohol acetyltransferase activity on flavor profiles of wine and distillates. Appl Environ Microbiol 66: 744-753.
36. Lilly, M., Bauer, F.F., Lambrechts, M.G., Swiegers, J.H., Cozzolino, D., and Pretorius, I.S. (2006) The effect of increased yeast alcohol acetyltransferase and esterase activity on the flavour profiles of wine and distillates. Yeast 23: 641-659.
37. Malcorps, P., and Dufour, J.P. (1987) Ester synthesis by Saccharomyces cerevisiae - localization of the acetyl-CoA isoamyl alcohol acetyltransferase. J Inst Brew 93: 160.
38. Malcorps, P., and Dufour, J.P. (1992) Short-chain and medium-chain aliphatic ester synthesis in Saccharomyces cerevisiae. Eur J Biochem 210: 1015-1022.
39. Malcorps, P., Cheval, J.M., Jamil, S., and 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.
40. Marchesini, S., and Poirier, Y. (2003) Futile cycling of intermediates of fatty acid biosynthesis toward peroxisomal beta-oxidation in Saccharomyces cerevisiae. J Biol Chem 278: 32596-32601.
41. Mason, A.B., and Dufour, J.P. (2000) Alcohol acetyltransferases and the significance of ester synthesis in yeast. Yeast 16: 1287-1298.
42. Meilgaard, M.C. (1975) Flavor chemistry of beer: Part II: Flavor and threshold of 239 aroma volatiles. MBAA Techn Quart 12: 151-168.
43. Meilgaard, M.C. (1991) The flavor of beer. MBAA Techn Quart 28: 132-141.
44. Miller, A.C., Wolff, S.R., Bisson, L.F., and Ebeler, S.E. (2007) Yeast strain and nitrogen supplementation: dynamics of volatile ester production in Chardonnay juice fermentations. Am J Enol Vitic 58: 470-483.
45. Nagasawa, N., Bogaki, T., Iwamatsu, A., Hamachi, M., and 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.
46. Narendranath, N.V., Thomas, K.C., and Ingledew, W.M. (2001) Acetic acid and lactic acid inhibition of growth of Saccharomyces cerevisiae by different mechanisms. J Am Soc Brew Chem 59: 187-194.
47. Nordström, K. (1962) Formation of ethyl acetate in fermentation with brewer's yeast III. Participation of coenzyme A. J Inst Brew 68: 398-407.
48. Nordström, K. (1964) Formation of esters from acids by brewer's yeast. IV. Effect of higher fatty acids and toxicity of lower fatty acids. J Inst Brew 70: 233-238.
49. Nykanen, I., and Suomalainen, H. (1983) Formation of aroma compounds by yeast. In Aroma of Beer, Wine and Distilled Beverages. Nykanen, I., and Suomalainen, H. (eds). Dordrecht, The Netherlands: Reidel Publishing Company, pp. 3-16.
50. Nykanen, L. (1986) Formation and occurence of flavor compounds in wine and distilled beverages. Am J Enol Vitic 37: 84-96.
51. Nykanen, L., and Nykanen, I. (1977) Production of esters by different yeast strains in sugar fermentations. J Inst Brew 83: 30-31.
52. Ollis, D.L., Cheah, E., Cygler, M., Dijkstra, B., Frolow, F., Franken, S.M., et al. (1992) The alpha/beta-hydrolase fold. Protein Eng 5: 197-211.
53. Pampulha, M.E., and Loureiro-Dias, M.C. (2000) Energetics of the effect of acetic acid on growth of Saccharomyces cerevisiae. FEMS Microbiol Lett 184: 69-72.
54. Peddie, H.A.B. (1990) Ester formation in brewery fermentations. J Inst Brew 96: 327-331.
55. Pisarnitskii, A.F. (2001) Formation of wine aroma: tones and imperfections caused by minor components (review). Appl Biochem Microbiol 37: 552-560.
56. Rodriguez-Vargas, S., Sanchez-Garcia, A., Martinez-Rivas, J.M., Prieto, J.A., and Randez-Gil, F. (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. Appl Environ Microbiol 73: 110-116.
57. Rolland, F., Winderickx, J., and Thevelein, J.M. (2002) Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2: 183-201.
58. Sa-Correia, I., Dos Santos, S.C., Teixeira, M.C., Cabrito, T.R., and Mira, N.P. (2009) Drug:H(+) antiporters in chemical stress response in yeast. Trends Microbiol 17: 22-31.
59. Saerens, S.M.G., Verstrepen, K.J., Laere, V., Voet, S.D.M., Van Dijck, A.R.D., Delvaux, P., et al. (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.
60. Saerens, S.M., Verbelen, P.J., Vanbeneden, N., Thevelein, J.M., and Delvaux, F.R. (2008a) 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.
61. Saerens, S.M., Delvaux, F., Verstrepen, K.J., Van Dijck, P., Thevelein, J.M., and Delvaux, F.R. (2008b) Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol 74: 454-461.
62. Sumper, M. (1974) Control of fatty acid biosynthesis by longchain acyl-CoAs and by lipid membranes. Eur J Biochem 49: 469-475.
63. Suomalainen, H. (1981) Yeast esterases and aroma esters in alcoholic beverages. J Inst Brew 87: 296-300.
64. Swiegers, J.H., and Pretorius, I.S. (2005) Yeast modulation of wine flavor. Adv Appl Microbiol 57: 131-175.
65. Taylor, G.T., and Kirsop, B.H. (1977) The origin of medium chain length fatty acids present in beer. J Inst Brew 83: 241-243.
66. Thevelein, J.M. (1994) Signal-transduction in yeast. Yeast 10: 1753-1790.
67. Thurston, P.A., Quain, D.E., and Tubb, R.S. (1982) Lipidmetabolism and the regulation of volatile ester synthesis in Saccharomyces cerevisiae. J Inst Brew 88: 90-94.
68. Tiwari, R., Koffel, R., and Schneiter, R. (2007) An acetylation/ deacetylation cycle controls the export of sterols and steroids from S. cerevisiae. EMBO J 26: 5109-5119.
69. Vadali, R.V., Bennett, G.N., and San, K.Y. (2004a) Cofactor engineering of intracellular CoA/acetyl-CoA and its effect on metabolic flux redistribution in Escherichia coli. Metab Eng 6: 133-139.
70. Vadali, R.V., Bennett, G.N., and San, K.Y. (2004b) Applicability of CoA/acetyl-CoA manipulation system to enhance isoamyl acetate production in Escherichia coli. Metab Eng 6: 294-299.
71. Vasconcelles, M.J., Jiang, Y., McDaid, K., Gilooly, L.,Wretzel, S., Porter, D.L., et al. (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.
72. Verstrepen, K.J., Derdelinckx, G., Dufour, J.P., Winderickx, J., Thevelein, J.M., Pretorius, I.S., and Delvaux, F.R. (2003a) Flavor-active esters: adding fruitiness to beer. J Biosci Bioeng 96: 110-118.
73. Verstrepen, K.J., Van Laere, S.D.M., Vanderhaegen, B.M.P., Derdelinckx, G., Dufour, J.P., Pretorius, I.S., et al. (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.
74. Verstrepen, K.J., Derdelinckx, G., Dufour, J.P., Winderickx, J., Pretorius, I.S., Thevelein, J.M., and Delvaux, F.R. (2003c) 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.
75. Verstrepen, K.J., Van Laere, S.D.M., Vercammen, J., Derdelinckx, G., Dufour, J.P., Pretorius, I.S., et al. (2004) The Saccharomyces cerevisiae alcohol acetyl transferase Atf1p is localized in lipid particles. Yeast 21: 367-376.
76. Vilanova, M., Ugliano, M., Varela, C., Siebert, T., Pretorius, I.S., and Henschke, P.A. (2007) Assimilable nitrogen utilisation and production of volatile and non-volatile compounds in chemically defined medium by Saccharomyces cerevisiae wine yeasts. Appl Microbiol Biotechnol 77: 145-157.
77. Wakil, S.J., Stoops, J.K., and Joshi, V. (1983) Fatty acid synthesis and its regulation. Annu Rev Biochem 52: 537-579.
78. Yoshimoto, H., Fujiwara, D., Momma, T., Ito, C., Sone, H., Kaneko, Y., and 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.
79. Yoshioka, K., and Hashimoto, N. (1981) Ester formation by alcohol acetyltransferase from brewers yeast. Agr Biol Chem 45: 2183-2190.
80. Younis, O.S., and Stewart, G.G. (1998) Sugar uptake and subsequent ester and higher alcohol production by Saccharomyces cerevisiae. J Inst Brew 104: 255-264.
81. Younis, O.S., and Stewart, G.G. (1999) Effect of malt wort, very-high-gravity malt wort, and very-high-gravity adjunct wort on volatile production in Saccharomyces cerevisiae. J. Am Soc Brew Chem 57: 39-45.