Advertisement

Microbial formation of esters

  • Yong Cheol Park
  • Catherine Emily Horton Shaffer
  • George N. Bennett
Mini-Review

Abstract

Small aliphatic esters are important natural flavor and fragrance compounds and have numerous uses as solvents and as chemical intermediates. Besides the chemical or lipase-catalyzed formation of esters from alcohols and organic acids, small volatile esters are made by several biochemical routes in microbes. This short review will cover the biosynthesis of esters from acyl-CoA and alcohol condensation, from oxidation of hemiacetals formed from aldehydes and alcohols, and from the insertion of oxygen adjacent to the carbonyl group in a straight chain or cyclic ketone by Baeyer–Villiger monooxygenases. The physiological role of the ester-forming reactions can allow degradation of ketones for use as a carbon source and may play a role in detoxification of aldehydes or recycling cofactors. The enzymes catalyzing each of these processes have been isolated and characterized, and a number of genes encoding the proteins from various microbes have been cloned and functionally expressed. The use of these ester-forming organisms or recombinant organisms expressing the appropriate genes as biocatalysts in biotechnology to make specific esters and chiral lactones has been studied in recent years.

Keywords

Ester Aroma Microorganism Yeast Alcohol Monooxygenase 

Notes

Acknowledgments

The work was supported by the National Science Foundation grants BES-0418289, BES-0222691, and BES0118815 and the USDA-NSF Inter Agency Metabolic Engineering Program: USDA 2002-35505-1163 and a grant (code no. 20070301034013) from BioGreen 21 Program, Rural Development Administration, Republic of Korea. Dr. Park also acknowledges his former institution, the Center for Agricultural Biomaterials, Seoul National University, Seoul 151-921, South Korea.

References

  1. Adachi S, Kobayashi T (2005) Synthesis of esters by immobilized-lipase-catalyzed condensation reaction of sugars and fatty acids in water-miscible organic solvent. J Biosci Bioeng 99:87–94CrossRefGoogle Scholar
  2. Akoh CC, Lee GC, Shaw JF (2004) Protein engineering and applications of Candida rugosa lipase isoforms. Lipids 39:513–526CrossRefGoogle Scholar
  3. Alphand V, Carrea G, Wohlgemuth R, Furstoss R, Woodley JM (2003) Towards large-scale synthetic applications of Baeyer–Villiger monooxygenases. Trends Biotechnol 21:318–323CrossRefGoogle Scholar
  4. Armstrong DW, Yamazaki H (1984) Effect of iron and EDTA on ethyl acetate accumulation in Candida utilis. Biotechnol Lett 6:819–824CrossRefGoogle Scholar
  5. Baldwin CV, Woodley JM (2006) On oxygen limitation in a whole cell biocatalytic Baeyer–Villiger oxidation process. Biotechnol Bioeng 95:362–369CrossRefGoogle Scholar
  6. Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen FW, Bouwmeester HJ, Aharoni A (2004) Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiol 135:1865–1878CrossRefGoogle Scholar
  7. Brzostowicz PC, Blasko MS, Rouviere PE (2002) Identification of two gene clusters involved in cyclohexanone oxidation in Brevibacterium epidermidis strain HCU. Appl Microbiol Biotechnol 58:781–789CrossRefGoogle Scholar
  8. Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116CrossRefGoogle Scholar
  9. Cheesman MJ et al (2001) Purification and characterization of hexahistidine-tagged cyclohexanone monooxygenase expressed in Saccharomyces cerevisiae and Escherichia coli. Protein Expr Purif 21:81–86CrossRefGoogle Scholar
  10. Chen YC, Peoples OP, Walsh CT (1988) Acinetobacter cyclohexanone monooxygenase: gene cloning and sequence determination. J Bacteriol 170:781–789Google Scholar
  11. Clouthier CM, Kayser MM, Reetz MT (2006) Designing new Baeyer–Villiger monooxygenases using restricted CASTing. J Org Chem 71:8431–8437CrossRefGoogle Scholar
  12. Cooley M, Chhabra SR, Williams P (2008) N-Acylhomoserine lactone-mediated quorum sensing: a twist in the tail and a blow for host immunity. Chem Biol 15:1141–1147CrossRefGoogle Scholar
  13. Cordente AG, Swiegers JH, Hegardt FG, Pretorius IS (2007) Modulating aroma compounds during wine fermentation by manipulating carnitine acetyltransferases in Saccharomyces cerevisiae. FEMS Microbiol Lett 267:159–166CrossRefGoogle Scholar
  14. D'Auria JC, Chen F, Pichersky E (2002) Characterization of an acyltransferase capable of synthesizing benzylbenzoate and other volatile esters in flowers and damaged leaves of Clarkia breweri. Plant Physiol 130:466–476CrossRefGoogle Scholar
  15. D'Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J (2007) Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J 49:194–207CrossRefGoogle Scholar
  16. Davies R, Falkiner EA, Wilkerson JF, Peel JL (1951) Ester formation by yeasts. 1. Ethyl acetate formation by Hansenula species. Biochem J 49:58–61Google Scholar
  17. de Smidt O, du Preez JC, Albertyn J (2008) The alcohol dehydrogenases of Saccharomyces cerevisiae: a comprehensive review. FEMS Yeast Res 8:967–978CrossRefGoogle Scholar
  18. Doig SD, O'Sullivan LM, Patel S, Ward JM, Woodley JM (2001) Large scale production of cyclohexanone monooxygenase from Escherichia coli TOP10 pQR239. Enzyme Microb Technol 28:265–274CrossRefGoogle Scholar
  19. Doig SD et al (2002) Reactor operation and scale-up of whole cell Baeyer–Villiger catalyzed lactone synthesis. Biotechnol Prog 18:1039–1046CrossRefGoogle Scholar
  20. Donoghue NA, Norris DB, Trudgill PW (1976) The purification and properties of cyclohexanone oxygenase from Nocardia globerula CL1 and Acinetobacter NCIB 9871. Eur J Biochem 63:175–192CrossRefGoogle Scholar
  21. Du W, Li W, Sun T, Chen X, Liu D (2008) Perspectives for biotechnological production of biodiesel and impacts. Appl Microbiol Biotechnol 79:331–337CrossRefGoogle Scholar
  22. Dudareva N, D'Auria JC, Nam KH, Raguso RA, Pichersky E (1998) Acetyl-CoA:benzylalcohol acetyltransferase—an enzyme involved in floral scent production in Clarkia breweri. Plant J 14:297–304CrossRefGoogle Scholar
  23. Durrans TH (1971) Solvents, Eighthth edn. Chapman and Hall, LondonGoogle Scholar
  24. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A 101:1781–1785CrossRefGoogle Scholar
  25. Ferreira-Torres C, Micheletti M, Lye GJ (2005) Microscale process evaluation of recombinant biocatalyst libraries: application to Baeyer–Villiger monooxygenase catalysed lactone synthesis. Bioprocess Biosyst Eng 28:83–93CrossRefGoogle Scholar
  26. Forney FW, Markovetz AJ (1969) An enzyme system for aliphatic methyl ketone oxidation. Biochem Biophys Res Commun 37:31–38CrossRefGoogle Scholar
  27. Fraaije MW, Kamerbeek NM, Heidekamp AJ, Fortin R, Janssen DB (2004) The prodrug activator EtaA from Mycobacterium tuberculosis is a Baeyer–Villiger monooxygenase. J Biol Chem 279:3354–3360CrossRefGoogle Scholar
  28. Fraaije MW, Wu J, Heuts DP, van Hellemond EW, Spelberg JHJ, Janssen DB (2005) Discovery of a thermostable Baeyer–Villiger monooxygenase by genome mining. Appl Microbiol Biotechnol 66:393–400CrossRefGoogle Scholar
  29. Fraajie MW, Kamerbeek NM, van Berkel WJH, Janssen DB (2002) Identification of a Baeyer–Villiger monooxygenase sequence motif. FEBS Lett 518:43–47CrossRefGoogle Scholar
  30. Fredlund E (2004) Central carbon metabolism in the biocontrol yeast Pichia anomala: influence of oxygen limitation. In: Department of Microbiology. Swedish University of Agricultural Sciences, UppsalaGoogle Scholar
  31. Fredlund E, Blank LM, Schnurer J, Sauer U, Passoth V (2004a) Oxygen- and glucose-dependent regulation of central carbon metabolism in Pichia anomala. Appl Environ Microbiol 70:5905–5911CrossRefGoogle Scholar
  32. Fredlund E, Broberg A, Boysen ME, Kenne L, Schnurer J (2004b) Metabolite profiles of the biocontrol yeast Pichia anomala J121 grown under oxygen limitation. Appl Microbiol Biotechnol 64:403–409CrossRefGoogle Scholar
  33. Fredlund E, Druvefors UA, Olstorpe MN, Passoth V, Schnurer J (2004c) Influence of ethyl acetate production and ploidy on the anti-mould activity of Pichia anomala. FEMS Microbiol Lett 238:133–137Google Scholar
  34. 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 60:2786–2792Google Scholar
  35. 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 12:593–598CrossRefGoogle Scholar
  36. Fukuda K et al (1998a) Balance of activities of alcohol acetyltransferase and esterase in Saccharomyces cerevisiae is important for production of isoamyl acetate. Appl Environ Microbiol 64:4076–4078Google Scholar
  37. Fukuda K et al (1998b) Brewing properties of sake yeast whose EST2 gene encoding isoamyl acetate-hydrolyzing esterase was disrupted. J Ferment Bioeng 85:101–106CrossRefGoogle Scholar
  38. Gray WD (1949) Initial studies on the metabolism of Hansenula anomala (Hansen) Sydow. Amer J Botany 36:475–480CrossRefGoogle Scholar
  39. Hausinger RP (2007) New insights into acetone metabolism. J Bacteriol 189:671–673CrossRefGoogle Scholar
  40. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A 104:5467–5472CrossRefGoogle Scholar
  41. Hilker I, Gutierrez MC, Furstoss R, Ward J, Wohlgemuth R, Alphand V (2008) Preparative scale Baeyer–Villiger biooxidation at high concentration using recombinant Escherichia coli and in situ substrate feeding and product removal process. Nat Protoc 3:546–554CrossRefGoogle Scholar
  42. Hirata D, Aoki S, Watanabe KI, Tsukooka M, Suzuki T (1992) Stable overexpression of isoamyl alcohol by Saccharomyces cerevisiae with chromosome-integrated multicopy LEU4 genes. Biosci Biotechnol Biochem 56:1682–2683CrossRefGoogle Scholar
  43. Hirosawa I, Aritomi K, Hoshida H, Kashiwagi S, Nishizawa Y, Akada R (2004) Construction of a self-cloning sake yeast that overexpresses alcohol acetyltransferase gene by a two-step gene replacement protocol. Appl Microbiol Biotechnol 65:68–73CrossRefGoogle Scholar
  44. Holland D et al (2005) Developmental and varietal differences in volatile ester formation and acetyl-CoA: alcohol acetyl transferase activities in apple (Malus domestica Borkh.) fruit. J Agric Food Chem 53:7198–7203CrossRefGoogle Scholar
  45. Horton CE, Bennett GN (2006) Ester production in E. coli and C. acetobutylicum. Enzyme Microb Technol 38:937–943CrossRefGoogle Scholar
  46. Horton CE, Huang KX, Bennett GN, Rudolph FB (2003) Heterologous expression of the Saccharomyces cerevisiae alcohol acetyltransferase genes in Clostridium acetobutylicum and Escherichia coli for the production of isoamyl acetate. J Ind Microbiol Biotech 30:427–432CrossRefGoogle Scholar
  47. Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120CrossRefGoogle Scholar
  48. Iwaki H, Hasegawa Y, Wang S, Kayser MM, Lau PCK (1999a) Cloning and characterization of a gene cluster involved in cyclopentanol metabolism in comamonas sp. strain NCIMB 9872 and biotransformations effected by Escherichia coli-expressed cyclopentanone 1, 2-monooxygenase. Appl Environ Microbiol 68:5671–5684CrossRefGoogle Scholar
  49. Iwaki H, Hasegawa Y, Teraoka M, Tokuyama T, Bergeron H, Lau PCK (1999b) Identification of a transcriptional activator (ChnR) and a 6-oxohexanoate dehydrogenase (ChnE) in the cyclohexanol catabolic pathway in Acinetobacter sp. strain NCIMB 9871 and localization of the genes that encode them. Appl Environ Microbiol 65:5158–5162Google Scholar
  50. Iwaki H et al (2006) Pseudomonad cyclopentadecanone monooxygenase displaying an uncommon spectrum of Baeyer–Villiger oxidations of cyclic ketones. Appl Environ Microbiol 72:2707–2720CrossRefGoogle Scholar
  51. Jetter R, Kunst L (2008) Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J 54:670–683CrossRefGoogle Scholar
  52. Joseph B, Ramteke PW, Thomas G (2008) Cold active microbial lipases: some hot issues and recent developments. Biotechnol Adv 26:457–470CrossRefGoogle Scholar
  53. Kallel-Mhiri H, Engasser J-M, Miclo A (1993) Continuous ethyl acetate production by Kluyveromyces fragilis on whey permeate. Appl Microbiol Biotechnol 40:201–205CrossRefGoogle Scholar
  54. Kamerbeek NM, Janssen DB, van Berkel WJH, Fraaije MW (2003a) Baeyer–Villiger monooxygenases, an emerging family of flavin-dependent biocatalysts. Adv Synth Catal 345:1–12CrossRefGoogle Scholar
  55. Kamerbeek NM, Olsthoorn AJ, Fraaije MW, Janssen DB (2003b) Substrate specificity and enantioselectivity of 4-hydroxyacetophenone monooxygenase. Appl Environ Microbiol 69:419–426CrossRefGoogle Scholar
  56. Kataoka M, Honda K, Sakamoto K, Shimizu S (2007) Microbial enzymes involved in lactone compound metabolism and their biotechnological applications. Appl Microbiol Biotechnol 75:257–266CrossRefGoogle Scholar
  57. Kayser MM, Clouthier CM (2006) New bioorganic reagents: evolved cyclohexanone monooxygenase—why is it more selective? J Org Chem 71:8424–8430CrossRefGoogle Scholar
  58. Kirschner A, Bornscheuer UT (2008) Directed evolution of a Baeyer–Villiger monooxygenase to enhance enantioselectivity. Appl Microbiol Biotechnol 81:465–472CrossRefGoogle Scholar
  59. Kirschner A, Altenbuchner J, Bornscheuer UT (2007) Cloning, expression, and characterization of a Baeyer–Villiger monooxygenase from Pseudomonas fluorescens DSM 50106 in E. coli. Appl Microbiol Biotechnol 73:1065–1072CrossRefGoogle Scholar
  60. Kneller MB, Cheesman MJ, Rettie AE (2001) ESI- and MALDI MS analysis of cyclohexanone monooxygenase from Acinetobacter NCIB 9871. Biochem Biophys Res Commun 282:899–903CrossRefGoogle Scholar
  61. Kotani T, Yamamoto T, Yurimoto H, Sakai Y, Kato N (2003) Propane monooxygenase and NAD(+)-dependent secondary alcohol dehydrogenase in propane metabolism by Gordonia sp strain TY-5. Journal of Bacteriology 185:7120–7128CrossRefGoogle Scholar
  62. Kotani T, Yurimoto H, Kato N, Sakai Y (2007) Novel acetone metabolism in a propane-utilizing bacterium, Gordonia sp. strain TY-5. J Bacteriol 189:886–893CrossRefGoogle Scholar
  63. Kusano M, Sakai Y, Kato N, Yoshimoto H, Sone H, Tamai Y (1998a) Hemiacetal dehydrogenation activity of alcohol dehydrogenases in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 62:1956–1961CrossRefGoogle Scholar
  64. Kusano M, Sakai Y, Kato N, Yoshimoto H, Sone H, Tamai Y (1998b) Hemiacetal dehydrogenation activity of alcohol dehydrogenases in Saccharomyces cerevisiae. Bioscience Biotechnology and Biochemistry 62:1956–1961CrossRefGoogle Scholar
  65. Kusano M, Sakai Y, Kato N, Yoshimoto H, Tamai Y (1999) A novel hemiacetal dehydrogenase activity involved in ethyl acetate synthesis in Candida utilis. J Biosci Bioeng 87:690–692CrossRefGoogle Scholar
  66. Kyte BG, Rouviere P, Cheng Q, Stewart JD (2004) Assessing the substrate selectivities and enantioselectivities of eight novel Baeyer–Villiger monooxygenases toward alkyl-substituted cyclohexanones. J Org Chem 69:12–17CrossRefGoogle Scholar
  67. Laurema S, Erkama J (1968) Formation of ethyl acetate in Hansenula anomala. Acta Chem Scand 22:1482–1486CrossRefGoogle Scholar
  68. Lee DH, Kim MD, Lee WH, Kweon DH, Seo JH (2004) Consortium of fold-catalyzing proteins increases soluble expression of cyclohexanone monooxygenase in recombinant Escherichia coli. Appl Microbiol Biotechnol 63:549–552CrossRefGoogle Scholar
  69. Lee WH, Park YC, Lee DH, Park K, Seo JH (2005) Simultaneous biocatalyst production and Baeyer–Villiger oxidation for bioconversion of cyclohexanone by recombinant Escherichia coli expressing cyclohexanone monooxygenase. Appl Biochem Biotechnol 121–124:827–836CrossRefGoogle Scholar
  70. Lee WH, Park JB, Park K, Kim MD, Seo JH (2007) Enhanced production of epsilon-caprolactone by overexpression of NADPH-regenerating glucose 6-phosphate dehydrogenase in recombinant Escherichia coli harboring cyclohexanone monooxygenase gene. Appl Microbiol Biotechnol 76:329–338CrossRefGoogle Scholar
  71. Leskovac V, Trivic S, Pericin D (2002) The three zinc-containing alcohol dehydrogenases from baker's yeast. Saccharomyces cerevisiae. FEMS Yeast Res 2:481–494Google Scholar
  72. 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 23:641–659CrossRefGoogle Scholar
  73. Magor AM, Warburton J, Trower MK, Griffin M (1986) Comparative study of the ability of three Xanthobacter species to metabolize cycloalkanes. Appl Environ Microbiol 52:665–671Google Scholar
  74. Malito E, Alfieri A, Fraaije MW, Mattevi A (2004) Crystal structure of a Baeyer–Villiger monooxygenase. Proc Natl Acad Sci U S A 101:13157–13162CrossRefGoogle Scholar
  75. Martinez I, Zhu J, Lin H, Bennett GN, San KY (2008) Replacing Escherichia coli NAD-dependent glyceraldehyde 3-phosphate dehydrogenase (GAPDH) with a NADP-dependent enzyme from Clostridium acetobutylicum facilitates NADPH dependent pathways. Metab Eng 10:352–359CrossRefGoogle Scholar
  76. Mason AB, Dufour J (2000) Alcohol acetyltransferases and the significance of ester synthesis in yeast. Yeast 16:1287–1298CrossRefGoogle Scholar
  77. Mihovilovic MD et al (2001) Asymmetric Baeyer–Villiger oxidations of 4-mono- and 4, 4-disubstituted cyclohexanones by whole cells of engineered Escherichia coli. J Org Chem 66:733–738CrossRefGoogle Scholar
  78. Mihovilovic MD, Rudroff F, Winninger A, Schneider T, Schulz F, Reetz MT (2006) Microbial Baeyer–Villiger oxidation: stereopreference and substrate acceptance of cyclohexanone monooxygenase mutants prepared by directed evolution. Org Lett 8:1221–1224CrossRefGoogle Scholar
  79. Møller K, Christensen B, Förster J, Piskur J, Nielsen J, Olsson L (2002) Aerobic glucose metabolism of Saccharomyces kluyveri: growth, metabolite production, and quantification of metabolic fluxes. Biotechnol Bioeng 77:186–193CrossRefGoogle Scholar
  80. Murdanoto AP, Sakai Y, Konishi T, Yasuda F, Tani Y, Kato N (1997a) Purification and properties of methyl formate synthase, a mitochondrial alcohol dehydrogenase, participating in formaldehyde oxidation in methylotrophic yeasts. Appl Environ Microbiol 63:1715–1720Google Scholar
  81. Murdanoto AP, Sakai Y, Sembiring L, Tani Y, Kato N (1997b) Ester synthesis by NAD(+)-dependent dehydrogenation of hemiacetal: production of methyl formate by cells of methylotrophic yeasts. Biosci Biotechnol Biochem 61:1391–1393CrossRefGoogle Scholar
  82. Nordström K (1962) Formation of ethyl acetate in fermentation with brewer's yeast. III. Participation of coenzyme A. J Inst Brew 68:398–407Google Scholar
  83. Nordström K (1964) Formation of esters from acids by brewer's yeast. J Inst Brew 70:233–242Google Scholar
  84. Onaca C, Kieninger M, Engesser KH, Altenbuchner J (2007) Degradation of alkyl methyl ketones by Pseudomonas veronii MEK700. J Bacteriol 189:3759–3767CrossRefGoogle Scholar
  85. Ottolina G, de Gonzolo G, Carrea G, Danieli B (2005) Enzymatic Baeyer–Villiger oxidation of bicyclic diketones. Adv Synth Catal 347:1035–1040CrossRefGoogle Scholar
  86. Park YC, Yun NR, San KY, Bennett GN (2006) Molecular cloning and characterization of the alcohol dehydrogenase ADH1 gene of Candida utilis ATCC9950. J Ind Microbiol Biotechnol 33:1032–1036CrossRefGoogle Scholar
  87. Park J, Kim D, Kim S, Kim J, Bae K, Lee C (2007a) The analysis and application of a recombinant monooxygenase library as a biocatalyst for the Baeyer–Villiger reaction. J Microbiol Biotechnol 17:1083–1089Google Scholar
  88. Park YC, San KY, Bennett GN (2007b) Characterization of alcohol dehydrogenase 1 and 3 from Neurospora crassa FGSC2489. Appl Microbiol Biotechnol 76:349–356CrossRefGoogle Scholar
  89. Passoth V, Fredlund E, Druvefors UA, Schnurer J (2006) Biotechnology, physiology and genetics of the yeast Pichia anomala. FEMS Yeast Res 6:3–13CrossRefGoogle Scholar
  90. Pastore GM, Sato HH, Yang TS, Park YK, Min DB (1994) Production of fruity aroma by newly isolated yeast. Biotechnol Lett 16:389–392CrossRefGoogle Scholar
  91. Pastore GM, Park YK, Min DB (1995) Production of fruity aroma by Neurospora species isolated from Beiju. Revista De Microbiologia 26:55–58Google Scholar
  92. Patel RN, Hou CT, Laskin AI, Derelanko P, Felix A (1979) Oxidation of secondary alcohols to methyl ketones by yeasts. Appl Environ Microbiol 38:219–223Google Scholar
  93. Peel JL (1951) Ester formation by yeasts. 2. Formation of ethyl acetate by washed suspensions of Hansenula anomala. Biochem J 49:62–67Google Scholar
  94. Quilter MG, Hurley JC, Lynch FJ, Murphy MG (2003) The production of isoamyl acetate from amyl alcohol by Saccharomyces cerevisiae. J Inst Brew 109:34–40Google Scholar
  95. Rehdorf J, Kirschner A, Bornscheuer UT (2007) Cloning, expression and characterization of a Baeyer–Villiger monooxygenase from Pseudomonas putida KT2440. Biotech Letters 29:1393–1398CrossRefGoogle Scholar
  96. Rehdorf J, Zimmer CL, Bornscheuer UT (2009) Cloning, expression, characterization and biocatalytic investigation of the 4-hydroxyacetophenone monooxygenase from Pseudomonas putida JD1. Appl Environ Microbiol 75:3106–3114CrossRefGoogle Scholar
  97. Reid MF, Fewson CA (1994) Molecular characterization of microbial alcohol dehydrogenases. Crit Rev Microbiol 20:13–56CrossRefGoogle Scholar
  98. Rojas V, Gil JV, Pinaga F, Manzanares P (2001) Studies on acetate ester production by non-saccharomyces wine yeasts. Int J Food Microbiol 70:283–289CrossRefGoogle Scholar
  99. Rojas V, Gil JV, Manzanares P, Gavara R, Piñaga F, Flors A (2002) Measurement of alcohol acetyltransferase and ester hydrolase activities in yeast extracts. Enzyme Microb Technol 30:224–230CrossRefGoogle Scholar
  100. Rojas V, Gil JV, Pinaga F, Manzanares P (2003) Acetate ester formation in wine by mixed cultures in laboratory fermentations. Int J Food Microbiol 86:181–188CrossRefGoogle Scholar
  101. Ryerson CC, Ballou DP, Walsh C (1982) Mechanistic studies on cyclohexanone oxygenase. Biochemistry 21:2644–2655CrossRefGoogle Scholar
  102. Saerens SM 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 281:4446–4456CrossRefGoogle Scholar
  103. Sakai Y, Murdanoto AP, Sembiring L, Tani Y, Kato N (1995) A novel formaldehyde oxidation pathway in methylotrophic yeasts—methylformate as a possible intermediate. FEMS Microbiol Lett 127:229–234CrossRefGoogle Scholar
  104. Salas JJ (2004) Characterization of alcohol acyltransferase from olive fruit. J Agric Food Chem 52:3155–3158CrossRefGoogle Scholar
  105. Shalit M et al (2001) Acetyl-coa: alcohol acetyltransferase activity and aroma formation in ripening melon fruits. J Agric Food Chem 49:794–799CrossRefGoogle Scholar
  106. Shalit M et al (2003) Volatile ester formation in roses. Identification of an acetyl-coenzyme A. Geraniol/Citronellol acetyltransferase in developing rose petals. Plant Physiol 131:1868–1876CrossRefGoogle Scholar
  107. Sheng D, Ballou DP, Massey V (2001) Mechanistic studies of cyclohexanone monooxygenase: chemical properties of intermediates involved in catalysis. Biochemistry 40:11156–11167CrossRefGoogle Scholar
  108. Singh V, Solanki K, Gupta MN (2008) Process optimization for biodiesel production. Recent Pat Biotechnol 2:130–143CrossRefGoogle Scholar
  109. Stewart JE, Kallio RE (1959) Bacterial hydrocarbon oxidation II. Ester formation from alkanes. J Bacteriol 78:726–730Google Scholar
  110. Stoveken T, Steinbuchel A (2008) Bacterial acyltransferases as an alternative for lipase-catalyzed acylation for the production of oleochemicals and fuels. Angew Chem Int Ed Engl 47:3688–3694CrossRefGoogle Scholar
  111. Szolkowy C, Eltis LD, Bruce NC, Grogan G (2009) Insights into sequence-activity relationships amongst Baeyer–Villiger monooxygenases as revealed by the intragenomic complement of enzymes from Rhodococcus jostii RHA1. Chembiochem 10:1208–1217CrossRefGoogle Scholar
  112. Tabachnick J, Joslyn MA (1953a) Formation of esters by yeast I. The production of ethyl acetate by standing surface cultures of Hansenula anomala. J Bact 65:1–9CrossRefGoogle Scholar
  113. Tabachnick J, Joslyn MA (1953b) Formation of esters by yeast. II. Investigations with cellular suspensions of Hansenula anomala. Plant Physiol 28:681–692CrossRefGoogle Scholar
  114. Tanner A, Hopper DJ (2000) Conversion of 4-hydroxyacetophenone into 4-phenyl acetate by a flavin adenine dinucleotide-containing Baeyer–Villiger-type monooxygenase. J Bacteriol 182:6565–6569CrossRefGoogle Scholar
  115. Tominaga T, Okuzawa Y, Kato S, Suzuki M (2003) The first isolation of two types of trifluoroleucine resistant mutants of Saccharomyces servazzii. Biotechnol Lett 25:1735–1738CrossRefGoogle Scholar
  116. Torres Pazmino DE, Baas BJ, Janssen DB, Fraaije MW (2008) Kinetic mechanism of phenylacetone monooxygenase from Thermobifida fusca. Biochemistry 47:4082–4093CrossRefGoogle Scholar
  117. Trower MK, Buckland RM, Griffin M (1989) Characterization of an FMN-containing cyclohexanone monooxygenase from a cyclohexane-grown Xanthobacter sp. Eur J Biochem 181:199–206CrossRefGoogle Scholar
  118. Vadali RV, Bennett GN, San KY (2004a) Applicability of CoA/acetyl-CoA manipulation system to enhance isoamyl acetate production in Escherichia coli. Metab Eng 6:294–299CrossRefGoogle Scholar
  119. Vadali RV, Horton CE, Rudolph FB, Bennett GN, San KY (2004b) Production of isoamyl acetate in ackA-pta and/or ldh mutants of Escherichia coli with overexpression of yeast ATF2. Appl Microbiol Biotechnol 63:698–704CrossRefGoogle Scholar
  120. Van Beilen JB et al (2003) Cloning of Baeyer–Villiger monooxygenases from Comamonas, Xanthobacter and Rhodococcus using polymerase chain reaction with highly degenerate primers. Environ Microbiol 5:174–182CrossRefGoogle Scholar
  121. Van Laere S, Saerens S, Verstrepen K, Van Dijck P, Thevelein J, Delvaux F (2008) Flavour formation in fungi: characterisation of KlAtf, the Kluyveromyces lactis orthologue of the Saccharomyces cerevisiae alcohol acetyltransferases Atf1 and Atf2. Appl Microbiol Biotechnol 78:783–792CrossRefGoogle Scholar
  122. Verbelen PJ, Saerens SM, Van Mulders SE, Delvaux F, Delvaux FR (2009) The role of oxygen in yeast metabolism during high cell density brewery fermentations. Appl Microbiol Biotechnol 82:1143–1156CrossRefGoogle Scholar
  123. Verduyn C, Breedveld GJ, Scheffers WA, Vandijken JP (1988) Substrate-specificity of alcohol dehydrogenase from the yeasts Hansenula polymorpha CBS 4732 and Candida utilis CBS 621. Yeast 4:143–148CrossRefGoogle Scholar
  124. Verma ML, Azmi W, Kanwar SS (2008) Microbial lipases: at the interface of aqueous and non-aqueous media. A review. Acta Microbiol Immunol Hung 55:265–294CrossRefGoogle Scholar
  125. Verstrepen KJ et al (2003a) Flavor-active esters: adding fruitiness to beer. J Biosci Bioeng 96:110–118Google Scholar
  126. Verstrepen KJ 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 69:5228–5237CrossRefGoogle Scholar
  127. Verstrepen KJ et al (2004) The Saccharomyces cerevisiae alcohol acetyl transferase Atf1p is localized in lipid particles. Yeast 21:367–377CrossRefGoogle Scholar
  128. Volker A, Kirschner A, Bornscheuer UT, Altenbuchner J (2008) Functional expression, purification, and characterization of the recombinant Baeyer–Villiger monooxygenase MekA from Pseudomonas veronii MEK700. Appl Microbiol Biotechnol 77:1251–1260CrossRefGoogle Scholar
  129. Walton AZ, Stewart JD (2002) An efficient enzymatic Baeyer–Villiger oxidation by engineered Escherichia coli cells under non-growing conditions. Biotechnol Prog 18:262–268CrossRefGoogle Scholar
  130. Walton AZ, Stewart JD (2004) Understanding and improving NADPH-dependent reactions by nongrowing Escherichia coli cells. Biotechnol Prog 20:403–411CrossRefGoogle Scholar
  131. Willetts A (1997) Structural studies and synthetic applications of Baeyer–Villiger monooxygenases. Trends Biotechnol 15:55–62CrossRefGoogle Scholar
  132. Yamauchi H, Hasuo T, Amachi T, Akita O, Hara S, Yoshizawa K (1989a) Cell-free synthesis of ethyl hexanoate by extract from Neurospora sp, containing a novel acyl coenzyme A-alcohol acyltransferase. Agric Biol Chem 53:821–825Google Scholar
  133. Yamauchi H, Hasuo T, Amachi T, Akita O, Hara S, Yoshizawa K (1989b) Purification and characterization of acyl coenzyme A-alcohol acyltransferase of Neurospora sp. Agric Biol Chem 53:1551–1556Google Scholar
  134. Yilmaztekin M, Erten H, Cabaroglu T (2008) Production of isoamyl acetate from sugar beet molasses by Williopsis saturnus var. saturnus. J Inst Brew 114:34–38Google Scholar
  135. Yoshimoto H et al (1999) Isolation and characterization of the ATF2 gene encoding alcohol acetyltransferase II in the bottom fermenting yeast Saccharomyces pastorianus. Yeast 15:409–417CrossRefGoogle Scholar
  136. Yoshimoto H, Fujiware D, Bogaki T, Nagasawa N, Fujii T (2001) Mechanisms of acetate ester production and control in yeasts. J Biosci Bioeng 91:231–231CrossRefGoogle Scholar
  137. Yoshioka K, Hashimoto N (1981) Ester formation by alcohol acetyltransferase from brewers' yeast. Agric Biol Chem 45:2183–2190Google Scholar
  138. Yoshizawa K, Yamauchi H, Hasuo T, Akita O, Hara S (1988) Production of a fruity odor by Neurospora sp. Agric Biol Chem 52:2129–2130Google Scholar
  139. Yurimoto H, Lee B, Yasuda F, Sakai Y, Kato N (2004) Alcohol dehydrogenases that catalyse methyl formate synthesis participate in formaldehyde detoxification in the methylotrophic yeast Candida boidinii. Yeast 21:341–350CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Yong Cheol Park
    • 1
  • Catherine Emily Horton Shaffer
    • 2
  • George N. Bennett
    • 3
  1. 1.Department of General EducationKookmin UniversitySeoulSouth Korea
  2. 2.Microbiology and Biochemistry, Department of Natural SciencesUniversity of HoustonHoustonUSA
  3. 3.Department of Biochemistry and Cell BiologyRice UniversityHoustonUSA

Personalised recommendations