Studies on the mechanism of synthesis of ethyl acetate in Kluyveromyces marxianus DSM 5422

Applied Microbiology and Biotechnology

Volumn 99, Issue 3, 2015, Pages 1131-1144

  Löser, Christian ^a   Urit, Thanet ^a,b   Keil, Peter ^a   Bley, Thomas ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b NAKHON SAWAN RAJABHAT UNIVERSITY   (Thailand)

Author keywords

Antimycin A; Carboxin; Cyanide; Ethyl acetate; Kluyveromyces marxianus; Oxygen

Indexed keywords

COPPER; CYANIDES; ELECTRON TRANSPORT PROPERTIES; ESTERS; ETHANOL; METAL RECOVERY; OXYGEN; OXYGEN SUPPLY; SYNTHESIS (CHEMICAL);

ANTIMYCIN A; CARBOXIN; ELECTRON TRANSPORT CHAIN; ENVIRONMENTALLY FRIENDLY SOLVENTS; ETHYL ACETATES; KLUYVEROMYCES MARXIANUS; SUCCINATE DEHYDROGENASE; TERMINAL ELECTRON ACCEPTORS;

IRON COMPOUNDS;

ACETIC ACID ETHYL ESTER; ALCOHOL; ANTIMYCIN A1; COPPER; CYANIDE; CYTOCHROME C OXIDASE; DISSOLVED OXYGEN; FUMARIC ACID; LACTOSE; MALONIC ACID; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; TRACE ELEMENT; UBIQUINOL CYTOCHROME C REDUCTASE; ACETIC ACID DERIVATIVE; IRON;

ACIDIFICATION; ALCOHOL CONSUMPTION; ALCOHOL PRODUCTION; AMMONIUM UPTAKE; ARTICLE; BIOMASS; BIOREACTOR; FERMENTATION; FUNGUS GROWTH; KLUYVEROMYCES MARXIANUS; METABOLISM; NONHUMAN; OXYGEN CONSUMPTION; PRODUCT RECOVERY; RESPIRATORY CHAIN; SUGAR INTAKE; SYNTHESIS; AEROBIC METABOLISM; ANAEROBIC GROWTH; CARBOHYDRATE METABOLISM; ELECTRON TRANSPORT; GENETICS; KLUYVEROMYCES; OXIDATION REDUCTION REACTION;

ACETATES; AEROBIOSIS; ANAEROBIOSIS; CARBOHYDRATE METABOLISM; COPPER; ELECTRON TRANSPORT; ETHANOL; IRON; KLUYVEROMYCES; METABOLIC NETWORKS AND PATHWAYS; OXIDATION-REDUCTION;

EID: 84925465523     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6098-4     Document Type: Article

References (91)

1. Abdel-Banat BMA, Hoshida H, Ano A, Nonklang S, Akada R (2010) High-temperature fermentation: how can processes for ethanol production at high temperatures become superior to the traditional process using mesophilic yeast? Appl Microbiol Biotechnol 85:861–867
2. Alexander NA, Jeffries TW (1990) Respiratory efficiency and metabolite partitioning as regulatory phenomena in yeasts. Enzym Microb Technol 12:2–19
3. Aoki S, Ito-Kuwa S (1982) Respiration of Candida albicans in relation to its morphogenesis. Plant Cell Physiol 23:721–726
4. Armstrong DW, Yamazaki H (1984) Effect of iron and EDTA on ethyl acetate accumulation in Candida utilis. Biotechnol Lett 6:819–824
5. Armstrong DW, Martin SM, Yamazaki H (1984a) Production of ethyl acetate from dilute ethanol solutions by Candida utilis. Biotechnol Bioeng 26:1038–1041
6. Armstrong DW, Martin SM, Yamazaki H (1984b) Production of acetaldehyde from ethanol by Candida utilis. Biotechnol Lett 6:183–188
7. Bai FW, Anderson WA, Moo-Young M (2008) Ethanol fermentation technologies from sugar and starch feedstocks. Biotechnol Adv 26:89–105
8. Bajpai P, Margaritus A (1982) Ethanol inhibition kinetics of Kluyveromyces marxianus grown on Jerusalem Artichoke juice. Appl Environ Microbiol 44:1325–1329
9. Bakker BM, Overkamp KM, van Maris AJA, Kötter P, Luttik MAH, van Dijken JP, Pronk JT (2001) Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol Rev 25:15–37
10. Bol J, Knol W, ten Brik B (1987) Optimization of the production of ethyl acetate from ethanol by Hansenula anomala. Dechema Monogr 105:235–236
11. Büschges R, Bahrenberg G, Zimmermann M, Wolf K (1994) NADH:ubiquinone oxidoreductase in obligate aerobic yeasts. Yeast 10:475–479
12. Castrillo JI, Kaliterna J, Weusthuis RA, van Dijken JP, Pronk JT (1996) High-cell-density cultivation of yeasts on disaccharides in oxygen-limited batch cultures. Biotechnol Bioeng 49:621–628
13. Corzo G, Revah S, Christen P (1995) Effect of oxygen on the ethyl acetate production from continuous ethanol stream by Candida utilis in submerged cultures. Dev Food Sci 37B:1141–1154
14. Cuillel M (2009) The dual personality of ionic copper in biology. J Incl Phenom Macrocycl Chem 65:165–170
15. Davies R, Falkiner EA, Wilkinson JF, Peel JL (1951) Ester formation by yeasts 1. Ethyl acetate formation by Hansenula species. Biochem J 49:58–61
16. Downie JA, Garland PB (1973) An antimycin A- and cyanide-resistant variant of Candida utilis arising during copper-limited growth. Biochem J 134:1051–1061
17. Duboc P, von Stockar U (1998) Systematic errors in data evaluation due to ethanol stripping and water vaporization. Biotechnol Bioeng 58:428–439
18. Ferrero I, Viola A-M, Goffeau A (1981) Induction by glucose of an antimycin-insensitive, azide-sensitive respiration in the yeast Kluyveromyces lactis. Antonie Van Leeuwenhoek 47:11–24
19. Fonseca GG, Gombert AK, Heinzle E, Wittmann C (2007) Physiology of the yeast Kluyveromyces marxianus during batch and chemostat cultures with glucose as the sole carbon source. FEMS Yeast Res 7:422–435
20. Fonseca GG, Heinzle E, Wittmann C, Gombert AK (2008) The yeast Kluyveromyces marxianus and its biotechnological potential. Appl Microbiol Biotechnol 79:339–354
21. Fredlund E, Blank LM, Schnürer J, Sauer U, Passoth V (2004) Oxygen- and glucose-dependent regulation of central carbon metabolism in Pichia anomala. Appl Environ Microbiol 70:5905–5911
22. Ghaly AE, El-Taweel AA (1995) Effect of nutrient supplements addition on ethanol production from cheese whey using Candida pseudotropicalis under batch condition. Appl Biochem Biotechnol 53:107–131
23. González Siso MI (1996) The biotechnological utilization of cheese whey: a review. Bioresour Technol 57:1–11
24. Gray WD (1949) Initial studies on the metabolism of Hansenula anomala (Hansen) Sydow. Am J Bot 36:475–480
25. Grubb CF, Mawson AJ (1993) Effects of elevated solute concentrations on the fermentation of lactose by Kluyveromyces marxianus Y-113. Biotechnol Lett 15:621–626
26. Guimarães PMR, Teixeira JA, Domingues L (2010) Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorisation of cheese whey. Biotechnol Adv 28:375–384
27. Hack CJ, Marchant R (1998) Characterisation of a novel thermotolerant yeast, Kluyveromyces marxianus var marxianus: development of an ethanol fermentation process. J Ind Microbiol Biotechnol 20:323–327
28. Hederstedt L, Rutberg L (1981) Succinate dehydrogenase—a comparative review. Microbiol Rev 45:542–555
29. Holz M (2011) Gentechnische Optimierung der Hefe Yarrowia lipolytica zur biotechnologischen Produktion von Succinat. Dissertation, Dresden University of Technology, Dresden
30. Holz M, Barth G (2013) Effects of the fungicide carboxin on growth, succinate dehydrogenase activity and succinate production of the non-conventional yeast Yarrowia lipolytica. In: Proc Ann VAAM Conf 2013. Springer, Heidelberg, pp 155–156
31. Hortsch R, Löser C, Bley T (2008) A two-stage CSTR cascade for studying the effect of inhibitory and toxic substances in bioprocesses. Eng Life Sci 8:650–657
32. Kallel-Mhiri H, Miclo A (1993) Mechanism of ethyl acetate synthesis by Kluyveromyces fragilis. FEMS Microbiol Lett 111:207–212
33. Kallel-Mhiri H, Miclo A (1995) Kinetics of lactose transport in Kluyveromyces fragilis grown in a chemostat on diluted whey permeate. J Ind Microbiol 15:45–48
34. Kallel-Mhiri H, Engasser JM, Miclo A (1993) Continuous ethyl acetate production by Kluyveromyces fragilis on whey permeate. Appl Microbiol Biotechnol 40:201–205
35. Kerscher SJ (2000) Diversity and origin of alternative NADH:ubiquinone oxidoreductases. Biochim Biophys Acta 1459:274–283
36. Krebs HA, Gurin S, Eggleston LV (1952) The pathway of oxidation of acetate in baker’s yeast. Biochem J 51:614–628
37. 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 87:690–692
38. Lancaster CRD (2002) Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 1553:1–6
39. Lane MM, Morrissey JP (2010) Kluyveromyces marxianus: a yeast emerging from its sister’s shadow. Fungal Biol Rev 24:17–26
40. Laurema S, Erkama J (1968) Formation of ethyl acetate in Hansenula anomala. Acta Chem Scand 22:1482–1486
41. Lenaz G, Fato R, Formiggini G, Genova ML (2007) The role of coenzyme Q in mitochondrial electron transport. Mitochondrion 7S:S8–S33
42. Lertwattanasakul N, Shigemoto E, Rodrussamee N, Limtong S, Thanonkeo P, Yamada M (2009) The crucial role of alcohol dehydrogenase Adh3 in Kluyveromyces marxianus mitochondrial metabolism. Biosci Biotechnol Biochem 73:2720–2726
43. Levi S, Rovida E (2009) The role of iron in mitochondrial function. Biochim Biophys Acta 1790:629–636
44. Liti G, Wardrop FR, Cardinali G, Martini A, Walker GM (2001) Differential responses to antimycin A and expressions of the Crabtree effect in selected Klyuveromyces spp. Ann Microbiol 51:235–243
45. Lodolo EJ, O’Connor-Cox ESC, Axcell BC (1999) Evidence of antimycin-insensitive respiration in a commercial brewing yeast. J Inst Brew 105:35–43
46. Löser C, Schröder A, Deponte S, Bley T (2005) Balancing the ethanol formation in continuous bioreactors with ethanol stripping. Eng Life Sci 5:325–332
47. Löser C, Urit T, Nehl F, Bley T (2011) Screening of Kluyveromyces strains for the production of ethyl acetate: design and evaluation of a cultivation system. Eng Life Sci 11:369–381
48. Löser C, Urit T, Förster S, Stukert A, Bley T (2012) Formation of ethyl acetate by Kluyveromyces marxianus on whey during aerobic batch and chemostat cultivation at iron limitation. Appl Microbiol Biotechnol 96:685–696
49. Löser C, Urit T, Stukert A, Bley T (2013) Formation of ethyl acetate from whey by Kluyveromyces marxianus on a pilot scale. J Biotechnol 163:17–23
50. Löser C, Urit T, Bley T (2014) Perspectives for the biotechnological production of ethyl acetate by yeasts. Appl Microbiol Biotechnol 98:5397–5415
51. Lynen F (1943) Zum biologischen Abbau der Essigsäure. II. Die Wirkung von Malonsäure auf den Abbau der Essigsäure durch Hefe. Liebigs Ann Chem 554:40–68
52. Manjare SD, Ghoshal AK (2006a) Comparison of adsorption of ethyl acetate on activated carbon and molecular sieves 5A and 13X. J Chem Eng Data 51:1185–1189
53. Manjare SD, Ghoshal AK (2006b) Adsorption equilibrium studies for ethyl acetate vapor and E-Merck 13X molecular sieve system. Sep Purif Technol 51:118–125
54. Manjare SD, Ghoshal AK (2006c) Studies on adsorption of ethyl acetate vapor on activated carbon. Ind Eng Chem Res 45:6563–6569
55. Mathre DE (1971) Mode of action of oxathiin systemic fungicides. III. Effect on mitochondrial activities. Pestic Biochem Physiol 1:216–224
56. Mawson AJ (1994) Bioconversions for whey utilization and waste abatement. Bioresour Technol 47:195–203
57. Murray DB, Haynes K, Tomita M (2011) Redox regulation in respiring Saccharomyces cerevisiae. Biochim Biophys Acta 1810:945–958
58. Opekarová M, Sigler K (1987) Separation of transport and metabolic steps in the uptake of succinate by Kluyveromyces fragilis. Folia Microbiol 32:200–205
59. Overkamp KM, Bakker BM, Steensma HY, van Dijken JP, Pronk JT (2002) Two mechanisms for oxidation of cytosolic NADPH by Kluyveromyces lactis mitochondria. Yeast 19:813–824
60. Park YC, Shaffer CEH, Bennett GN (2009) Microbial formation of esters. Appl Microbiol Biotechnol 85:13–25
61. Pesta G, Meyer-Pittroff R, Russ W (2007) Utilization of whey. In: Oreopoulou V, Russ W (eds) Utilization of by-products and treatment of waste in the food industry. Springer, New York, pp 193–207
62. Posada JA, Patel AD, Roes A, Blok K, Faaij APC, Patel MK (2013) Potential of bioethanol as a chemical building block for biorefineries: preliminary sustainability assessment of 12 bioethanol-based products. Bioresour Technol 135:490–499
63. Prazeres AR, Carvalho F, Rivas J (2012) Cheese whey management: a review. J Environ Manag 110:48–68
64. Queiros O, Casal M, Althoff S, Moradas-Ferreira P, Leao C (1998) Isolation and characterization of Kluyveromyces marxianus mutants deficient in malate transport. Yeast 14:401–407
65. Rojas V, Gil JV, Piñaga F, Manzanares P (2001) Studies on acetate ester production by non-Saccharomyces wine yeasts. Int J Food Microbiol 70:283–289
66. Rojas V, Gil JV, Piñaga F, Manzanares P (2003) Acetate ester formation in wine by mixed cultures in laboratory fermentations. Int J Food Microbiol 86:181–188
67. Saliola M, Sponziello M, D’Amici S, Lodi T, Falcone C (2008) Characterization of KlGUT2, a gene of the glycerol-3-phosphate shuttle, in Kluyveromyces lactis. FEMS Yeast Res 8:697–705
68. Silveira WB, Passos FJV, Mantovani HC, Passos FML (2005) Ethanol production from cheese whey permeate by Kluyveromyces marxianus UFV-3: a flux analysis of oxidoreductive metabolism as a function of lactose concentration and oxygen levels. Enzym Microb Technol 36:930–936
69. Strong FM (1958) Topics in microbial chemistry. Wiley, New York
70. Szczodrak J, Szewcuk D, Rogalski J, Fiedurek J (1997) Selection of yeast strain and fermentation conditions for high-yield ethanol production from lactose and concentrated whey. Acta Biotechnol 17:51–61
71. Tabachnick J, Joslyn MA (1953) Formation of esters by yeast. I. The production of ethyl acetate by standing surface cultures of Hansenula anomala. J Bacteriol 65:1–9
72. Tarrío N, Becerra M, Cerdán ME, González Siso MI (2006) Reoxidation of cytosolic NADPH in Kluyveromyces lactis. FEMS Yeast Res 6:371–380
73. Taylor F, Kurantz MJ, Goldberg N, McAloon AJ, Craig JC (2000) Dry-grind process for fuel ethanol by continuous fermentation and stripping. Biotechnol Prog 16:541–547
74. Thomas KC, Dawson PSS (1978) Relationship between iron-limited growth and energy limitation during phased cultivation of Candida utilis. Can J Microbiol 24:440–447
75. Tin CSF, Mawson AJ (1993) Ethanol production from whey in a membrane recycle bioreactor. Process Biochem 28:217–221
76. Ulrich JT, Mathre DE (1972) Mode of action of oxathiin systemic fungicides. V. Effect on electron transport system of Ustilago maydis and Saccharomyces cerevisiae. J Bacteriol 110:628–632
77. Urit T, Löser C, Wunderlich M, Bley T (2011) Formation of ethyl acetate by Kluyveromyces marxianus on whey: studies of the ester stripping. Bioprocess Biosyst Eng 34:547–559
78. Urit T, Löser C, Stukert A, Bley T (2012) Formation of ethyl acetate by Kluyveromyces marxianus on whey during aerobic batch cultivation at specific trace-element limitation. Appl Microbiol Biotechnol 96:1313–1323
79. Urit T, Manthey R, Bley T, Löser C (2013a) Formation of ethyl acetate by Kluyveromyces marxianus on whey: influence of aeration and inhibition of yeast growth by ethyl acetate. Eng Life Sci 13:247–260
80. Urit T, Li M, Bley T, Löser C (2013b) Growth of Kluyveromyces marxianus and formation of ethyl acetate depending on temperature. Appl Microbiol Biotechnol 97:10359–10371
81. +-galactoside symport in the yeast Kluyveromyces marxianus. Biochem J 242:729–734
82. Veiga A, Arrabaça JD, Loureiro-Dias MC (2000) Cyanide-resistant respiration is frequent, but confined to yeasts incapable of aerobic fermentation. FEMS Microbiol Lett 190:93–97
83. Veiga A, Arrabaça JD, Sansonetty F, Ludovico P, Côrte-Real M, Loureiro-Dias MC (2003) Energy conversion coupled to cyanide-resistant respiration in the yeasts Pichia membranifaciens and Debaryomyces hansenii. FEMS Yeast Res 3:141–148
84. Verstrepen KJ, Van Laere SDM, Vercammen J, Derdelinckx G, Dufour J-P, Pretorius IS, Winderickx J, Thevelein JM, Delvaux FR (2004) The Saccharomyces cerevisiae alcohol acetyl transferase Atf1p is localized in lipid particles. Yeast 21:367–377
85. Vienne P, von Stockar U (1985a) Metabolic, physiological and kinetic aspects of the alcoholic fermentation of whey permeate by Kluyveromyces fragilis NRRL 665 and Kluyveromyces lactis NCYC 571. Enzym Microb Technol 7:287–294
86. Vienne P, von Stockar U (1985b) An investigation of ethanol inhibition and other limitations occurring during the fermentation of concentrated whey permeate by Kluyveromyces fragilis. Biotechnol Lett 7:521–526
87. Wallace KB, Starkov AA (2000) Mitochondrial targets of drug toxicity. Annu Rev Pharmacol Toxicol 40:353–388
88. Westall S (1998) Characterisation of yeast species by their production of volatile metabolites. J Food Mycol 1:187–201
89. Willetts A (1989) Ester formation from ethanol by Candida pseudotropicalis. Antonie Van Leeuwenhoek 56:175–180
90. Yong FM, Lee KH, Wong HA (1981) The production of ethyl acetate by soy yeast Saccharomyces rouxii NRRL Y-1096. J Food Technol 16:177–184
91. Zweytick D, Athenstaedt K, Daum G (2000) Intracellular lipid particles of eukaryotic cells. Biochim Biophys Acta 1469:101–120