Expression of Vitreoscilla hemoglobin improves the metabolism of xylose in recombinant yeast Saccharomyces cerevisiae under low oxygen conditions

Enzyme and Microbial Technology

Volumn 39, Issue 1, 2006, Pages 6-14

  Ruohonen, Laura ^a   Aristidou, Aristos ^a   Frey, Alexander D ^b   Penttilä, Merja ^a   Kallio, Pauli T ^b  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b ETH ZURICH   (Switzerland)

Author keywords

Ethanol; Saccharomyces cerevisiae; Vitreoscilla hemoglobin (VHb); Xylose

Indexed keywords

ETHANOL; FERMENTATION; GENES; GLUCOSE; METABOLISM; SACCHARIFICATION; STRAIN; SUGARS; XYLOSE; YEAST;

LIGNOCELLULOSIC MATERIALS; RECOMBINANT YEAST; SACCHAROMYCES CEREVISIAE; VITREOSCILLA HEMOGLOBIN (VHB);

HEMOGLOBIN;

ALCOHOL; CARBON; HEMOGLOBIN; OXYGEN; XYLITOL; XYLOSE;

ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; FERMENTATION; FUNGAL STRAIN; GENE EXPRESSION; HYPOXIA; NONHUMAN; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; VITREOSCILLA; YEAST;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE; VITREOSCILLA;

EID: 33646051550     PISSN: 01410229     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2005.06.024     Document Type: Article

References (66)

1. Gong C.S., Cao N.J., Du J., and Tsao G.T. Ethanol production from renewable resources. Adv Biochem Eng Biotechnol 65 (1999) 207-241
2. Hahn-Hägerdal B., Wahlbom C.F., Gárdonyi M., van Zyl W.H., Cordero Otero R.R., and Jönsson L. Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Adv Biochem Eng Biotechnol 73 (2001) 53-84
3. Barnett J.A. The utilization of sugars by yeasts. Adv Carbohydr Chem Biochem 32 (1976) 126-228
4. Aristidou A., and Penttilä M. Metabolic engineering applications to renewable resource utilization. Curr Opin Biotechnol 11 (2000) 187-198
5. Mielenz J.R. Ethanol production from biomass: technology and commercialization status. Curr Opin Microbiol 4 (2001) 324-329
6. Zaldivar J., Nielsen J., and Olsson L. Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56 (2001) 17-34
7. Jeffries T.W., and Jin Y.-S. Metabolic engineering for improved fermentation of pentoses by yeasts. Appl Microbiol Biotechnol 63 (2004) 495-509
8. Kötter P., Amore R., Hollenberg C.P., and Ciriacy M. Isolation and characterization of the Pichia stipitis xylitol dehydrogenase gene, XYL2, and construction of a xylose-utilizing Saccharomyces cerevisiae transformant. Curr Gen 38 (1990) 493-500
9. Kötter P., and Ciriacy M. Xylose fermentation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 38 (1993) 776-783
10. Ho N.W., Chen Z., and Brainard A.P. Genetically engineered Saccharomyces yeast capable of effective cofermentation of glucose and xylose. Appl Environ Microbiol 64 (1998) 1852-1859
11. Tantirungkij M., Nakashima N., Seki T., and Yoshida Y. Construction of xylose-assimilating Saccharomyces cerevisiae. J Ferment Bioeng 75 (1993) 83-88
12. Toivari M.H., Aristidou A., Ruohonen L., and Penttilä M. Conversion of xylose to ethanol by recombinant Saccharomyces cerevisiae: importance of xylulokinase (XKS1) and oxygen availability. Metab Eng 3 (2001) 236-249
13. Walfridsson M., Hallborn J., Penttilä M., Keränen S., and Hahn-Hägerdal B. Xylose-metabolizing Saccharomyces cerevisiae strains overexpressing the TKL1 and TAL1 genes encoding the pentose phosphate pathway enzymes transketolase and transaldolase. Appl Environ Microbiol 61 (1995) 4184-4190
14. Eliasson A., Christensson C., Wahlbom C.F., and Hahn-Hägerdal B. Anaerobic xylose fermentation by recombinant Saccharomyces cerevisiae carrying XYL1, XYL2 and XKS1 in mineral medium chemostat cultures. Appl Environ Microbiol 66 (2000) 3381-3386
15. Walfridsson M., Anderlund M., Bao X., and Hahn-Hägerdal B. Expression of different levels of enzymes from the Pichia stipitis XYL1 and XYL2 genes in Saccharomyces cerevisiae and its effects on product formation during xylose utilisation. Appl Microbiol Biotechnol 48 (1997) 218-224
16. Zaldivar J., Borges A., Johansson B., Smits H.P., Villas-Bôas S.G., Nielsen J., et al. Fermentation performance and intracellular metabolite patterns in laboratory and industrial xylose-fermenting Saccharomyces cerevisiae. Appl Microbiol Biotechnol 59 (2002) 436-442
17. Jin Y.-S., Ni H., Laplaza J.M., and Jeffries T.W. Optimal growth and ethanol production from xylose by recombinant Saccharomyces cerevisiae require moderate d-xylulokinase activity. Appl Environ Microbiol 69 (2003) 495-503
18. Johansson B., Christensson C., Hobley T., and Hahn-Hägerdal B. Xylulokinase overexpression in two strains of Saccharomyces cerevisiae also expressing xylose reductase and xylitol dehydrogenase and its effect on fermentation of xylose and lignocellulosic hydrolysate. Appl Environ Microbiol 67 (2001) 4249-4255
19. Bruinenberg P.M., de Bot P.H.M., van Dijken J.P., and Scheffers W.A. The role of redox balances in the anaerobic fermentation of xylose by yeasts. Eur J Appl Microbiol Biotechnol 18 (1983) 287-292
20. Bruinenberg P.M., de Bot P.H.M., van Dijken J.P., and Scheffers W.A. NADH-linked aldose reductase-key to anaerobic alcoholic fermentation of xylose by yeasts. Appl Microbiol Biotechnol 19 (1984) 256-260
21. Rizzi M., Erlemann P., Bui-Thanh N.A., and Dellweg H. Xylose fermentation by yeast. 4. Purification and kinetics of xylose reductase from Pichia stipitis. Appl Microbiol Biotechnol 29 (1988) 148-154
22. +-xylitol dehydrogenase from the yeast Pichia stipitis. J Ferment Bioeng 67 (1989) 20-24
23. Verduyn C., van Kleef R., Frank J., Schreuder H., van Dijken J.P., and Scheffers W.A. Properties of the NAD(P)H-dependent xylose reductase from the xylose-fermenting yeast Pichia stipitis. Biochem J 226 (1985) 669-677
24. Petschacher B., Leitgeb S., Kavanagh K.L., Wilson D.K., and Nidetzky B. The coenzyme specificity of Candida tenuis xylose reductase (AKR2B5) explored by site-directed mutagenesis and X-ray crystallography. Biochem J 385 (2005) 75-83
25. Watanabe S., Kodaki T., and Makino K. Complete reversal of coenzyme specificity of xylitol dehydrogenase and increase of thermostability by the introduction of structural zinc. J Biol Chem 280 (2005) 10340-10349
26. Aristidou A, Londesborough J, Penttilä M, Richard P, Ruohonen L, Söderlund H, et al. Transformed microorganisms with improved properties. 1999. PCT/FI99/00185, WO 99/46363.
27. Roca C., Nielsen J., and Olsson L. Metabolic engineering of ammonium assimilation in xylose-fermenting Saccharomyces cerevisiae improves ethanol production. Appl Environ Microbiol 69 (2003) 4732-4736
28. Verho R., Londesborough J., Penttilä M., and Richard P. Engineering redox cofactor regeneration for improved pentose fermentation in Saccharomyces cerevisiae. Appl Environ Microbiol 69 (2003) 5892-5897
29. +-xylitol dehydrogenase from the yeast Pichia stipitis. J Ferment Bioeng 67 (1989) 25-30
30. Eliasson A., Hofmeyer J.-H.S., Pedler S., and Hahn-Hägerdal B. The xylose reductase/xylitol dehydrogenase/xylulokinase ratio affects product formation in recombinant xylose-utilising Saccharomyces cerevisiae. Enzyme Microb Technol 29 (2001) 288-297
31. Jeppsson M., Johansson B., Hahn-Hägerdal B., and Gorwa-Grauslund M.F. Reduced oxidative pentose phosphate pathway flux in recombinant xylose-utilizing Saccharomyces cerevisiae strains improves the ethanol yield from xylose. Appl Environ Microbiol 68 (2002) 1604-1609
32. Jeppsson M., Träff K., Johansson B., Hahn-Hägerdal B., and Gorwa-Grauslund M.F. Effect of enhanced xylose reductase activity on xylose consumption and product distribution in xylose-fermenting recombinant Saccharomyces cerevisiae. FEMS Yeast Res 3 (2003) 167-175
33. Kuyper M., Harhangi H.R., Stave A.K., Winkler A.A., Jetten M.S.M., de Laat W.T.A.M., et al. High level functional expression of a fungal xylose isomerase; the key to efficient ethanolic fermentation of xylose of Saccahromyces cerevisiae?. FEMS Yeast Res 4 (2003) 69-78
34. Kuyper M., Winkler A.A., van Dijken J.P., and Pronk J.T. Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: a proof of principle. FEMS Yeast Res 4 (2004) 655-664
35. Pitkänen J.-P., Aristidou A., Salusjärvi L., Ruohonen L., and Penttilä M. Metabolic flux analysis of xylose metabolism in recombinant Saccharomyces cerevisiae using continuous culture. Metab Eng 5 (2003) 16-31
36. Bailey J.E., Sburlati A., Hatzimanikatis V., Lee K.H., Renner W.A., and Tsai P.S. Inverse metabolic engineering: a strategy for directed genetic engineering of useful phenotypes. Biotechnol Bioeng 52 (1996) 109-121
37. Konz J.O., King J., and Cooney C.L. Effects of oxygen on recombinant protein expression. Biotechnol Prog 14 (1998) 393-409
38. Moens L., Vanfleteren J., van de Peer Y., Peeters K., Kapp O., Czeluzniak J., et al. Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships. Mol Biol Evol 13 (1996) 324-333
39. Kallio P.T., Kim D.-J., Tsai P.S., and Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. Eur J Biochem 219 (1994) 201-208
40. Frey A.D., and Kallio P.T. Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiol Rev 27 (2003) 525-545
41. Chen W., Hughes D.E., and Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin alters the aerobic metabolism of Saccharomyces cerevisiae. Biotechnol Prog 10 (1994) 308-313
42. Farrés J., and Kallio P.T. Improved cell growth in tobacco suspension cultures expressing Vitreoscilla hemoglobin. Biotechnol Prog 18 (2002) 229-233
43. Häggman H., Frey A.D., Ryynänen L., Aronen T., Julkunen-Tiitto R., Tiimonen H., et al. Expression of Vitreoscilla hemoglobin in hybrid aspen (Populus tremula × tremuloides). Plant Biotechnol J 1 (2003) 287-300
44. 31P NMR and saturation transfer study. Biotechnol Prog 10 (1994) 360-364
45. Park K.W., Kim K.J., Howard A.J., Stark B.C., and Webster D.A. Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases. J Biol Chem 277 (2002) 33334-33337
46. Tsai P.S., Hatzimanikatis V., and Bailey J.E. Effect of Vitreoscilla hemoglobin dosage on microaerobic Escherichia coli carbon and energy metabolism. Biotechnol Bioeng 49 (1996) 139-150
47. Tsai P.S., Nägeli M., and Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin modifies microaerobic Escherichia coli metabolism through elevated concentration and specific activity of cytochrome o. Biotechnol Bioeng 49 (1996) 151-160
48. Tsai P.S., Rao G., and Bailey J.E. Improvement of Escherichia coli microaerobic oxygen metabolism by Vitreoscilla hemoglobin: new insights from NAD(P)H fluorescence and culture redox potential. Biotechnol Bioeng 47 (1995) 347-354
49. Boles E., Gohlmann H.W., and Zimmermann F.K. Cloning of a second gene encoding 5-phosphofructo-2-kinase in yeast, and characterization of mutant strains without fructose 2,6-bisphosphate. Mol Microbiol 20 (1996) 65-76
50. van Dijken J.P., Bauer J., Brambilla L., Duboc P., Francois J.M., Gancedo C., et al. An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains. Enzyme Microb Technol 26 (2000) 706-714
51. Ruohonen L., Aalto M.K., and Keränen S. Modifications to the ADH1 promoter of Saccharomyces cerevisiae for efficient production of heterologous proteins. J Biotechnol 39 (1995) 193-203
52. Richard P., Toivari M.H., and Penttilä M. The role of xylulokinase in Saccharomyces cerevisiae xylulose catabolism. FEMS Microbiol Lett 190 (2000) 39-43
53. Mellor J., Dobson M.J., Roberts N.A., Tuite M.F., Emtage J.S., White S., et al. Efficient synthesis of enzymatically active calf chymosin in Saccharomyces cerevisiae. Gene 24 (1983) 1-14
54. Gietz R.D., and Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenised yeast genes lacking six-base pair restriction sites. Gene 74 (1988) 527-534
55. Khosla C., and Bailey J.E. The Vitreoscilla hemoglobin gene: molecular cloning, nucleotide sequence and genetic expression in Escherichia coli. Mol Gen Genet 214 (1988) 158-161
56. Frey A.D., Bailey J.E., and Kallio P.T. Expression of Alcaligenes eutrophus flavohemoprotein and engineered Vitreoscilla hemoglobin-reductase fusion protein for improved hypoxic growth of Escherichia coli. Appl Environ Microbiol 66 (2000) 98-104
57. Sherman F., Fink G., and Hicks J.B. Methods in yeast genetics: a laboratory manual. (1983), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
58. Gietz R.D., St. Jean A., Woods R.A., and Schiestl R.H. Improved method for high efficiency transformation of intact yeast cells. Nucl Acids Res 20 (1992) 1425
59. Hill J., Donald K.A., Griffiths D.E., and Donald G. DMSO-enhanced whole cell yeast transformation. Nucl Acids Res 19 (1991) 5791 Published erratum appeared in Nucl Acids Res 1991;19:6688
60. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
61. Laemmli U.K. Cleavage of structural proteins during the assembly of the head bacteriophage T4. Nature 277 (1970) 680-685
62. Bollinger C.J.T., Bailey J.E., and Kallio P.T. Novel hemoglobins to enhance microaerobic growth and substrate utilization in Escherichia coli. Biotechnol Prog 17 (2001) 798-808
63. 0 mutant reveals the existence of a novel acetaldehyde-reducing activity in Saccharomyces cerevisiae. J Bacteriol 172 (1990) 3909-3917
64. Skoog K., and Hahn-Hägerdal B. Effect of oxygenation on xylose fermentation by Pichia stipitis. Appl Environ Microbiol 56 (1990) 3389-3394
65. 13C} xylose metabolism in Pichia stipitis under aerobic and anaerobic conditions. Appl Microbiol Biotechnol 28 (1988) 293-296
66. Wahlbom C.F., Eliasson A., and Hahn-Hägerdal B. Intracellular fluxes in a recombinant xylose-utilizing Saccharomyces cerevisiae cultivated anaerobically at different dilution rates and feed concentrations. Biotechnol Bioeng 72 (2001) 289-296