Elucidation of a carotenoid biosynthesis gene cluster encoding a novel enzyme, 2,2′-β-hydroxylase, from Brevundimonas sp. strain SD212 and combinatorial biosynthesis of new or rare xanthophylls

Applied and Environmental Microbiology

Volumn 71, Issue 8, 2005, Pages 4286-4296

  Nishida, Yasuhiro ^a   Adachi, Kyoko ^b   Kasai, Hiroaki ^b   Shizuri, Yoshikazu ^b   Shindo, Kazutoshi ^c   Sawabe, Akiyoshi ^a   Komemushi, Sadao ^a   Miki, Wataru ^d   Misawa, Norihiko ^b  

^a KINKI UNIVERSITY   (Japan)

^b MARINE BIOTECHNOLOGY INSTITUTE   (Japan)

^c Tokyo Women's Medical University   (Japan)

^d SUNTORY LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATMOSPHERIC PRESSURE; BACTERIA; BIOSYNTHESIS; DNA; ENZYMES; ESCHERICHIA COLI; IONIZATION; MASS SPECTROMETRY; PHOTODETECTORS;

CAROTENOID BIOSYNTHESIS; GENE CLUSTER; INHIBITORY EFFECT; SEQUENCE ANALYSIS;

GENES;

2 HYDROXYASTAXANTHIN; ACYL COENZYME A DESATURASE; ASTAXANTHIN; CANTHAXANTHIN; CAROTENOID; CAROTENOID 2,2' BETA HYDROXYLASE; OXYGENASE; STEROL; STEROL C5 DESATURASE; UNCLASSIFIED DRUG; XANTHOPHYLL; ZEAXANTHIN;

MICROBIOLOGY;

ARTICLE; BACTERIAL GENE; BACTERIOPLANKTON; BIOSYNTHESIS; BREVUNDIMONAS; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; GENE CLUSTER; GENETIC COMPLEMENTATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID PEROXIDATION; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BIOTECHNOLOGY; CAROTENOIDS; CAULOBACTERACEAE; ESCHERICHIA COLI; HUMANS; MICE; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; XANTHOPHYLLS;

ANIMALIA; BACTERIA (MICROORGANISMS); BREVUNDIMONAS; ESCHERICHIA COLI;

EID: 23744476402     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.8.4286-4296.2005     Document Type: Article

References (56)

1. Albrecht, M., N. Misawa, and G. Sandmann. 1999. Metabolic engineering of the terpenoid biosynthetic pathway of Escherichia coli for production of the carotenoids β-carotene and zeaxanthin. Biotechnol. Lett. 21:791-795.
2. The Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group. 1994. The effect of vitamin E and β-carotene on the incidence of lung cancer and other cancers in male smokers. N. Engl. J. Med. 330:1029-1035.
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipmann. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Armstrong, G. A., M. Alberti, and J. E. Hearst. 1990. Conserved enzymes mediate the early reactions of carotenoid biosynthesis in nonphotosynthetic and photosynthetic prokaryotes. Proc. Natl. Acad. Sci. USA 87:9975-9979.
5. Armstrong, G. A., and J. E. Hearst. 1996. Genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J. 10:228-237.
6. Berry, A., D. Janssens, M. Humbelin, J. P. M. Jore, B. Hoste, I. Cleenwerck, M. Vancanneyt, W. Bretzel, A. F. Mayer, R. Lopez-Ulibarri, B. Shanmugam, J. Swings, and L. Pasmontes. 2003. Pamcoccus zeaxanthinifaciens sp. nov., a zeaxanthin-producing bacterium. Int. J. Syst. Evol. Microbiol. 53:231-238.
7. Bertram, J. S. 1999. Carotenoids and gene regulation. Nutr. Rev. 57:182-191.
8. Britton, G., S. Liaaen-Jensen, and H. Pfander. 2004. Carotenoids handbook. Birkhauser Verlag, Basel, Switzerland.
9. Chamovitz, D., N. Misawa, G. Sandmann, and J. Hirschberg. 1992. Molecular cloning and expression in Escherichia coli of a cyanobacterial gene coding for phytoene synthase, a carotenoid biosynthesis enzyme. FEBS Lett. 296:305-310.
10. Farmer, W. R., and J. C. Liao. 2000. Improving lycopenc production in Escherichia coli by engineering metabolic control. Nat. Biotechnol. 18:533-537.
11. Foss, P., V. Partali, Y. Olsen, G. Borch, and S. Liaaen-Jensen. 1986. Animal carotenoids 29*. New (2R)-2-hydroxy-4-keto-β-type carotenoids from Daphnia magna (Crustaceae). Acta Chem. Scand. B 40:157-162.
12. Fraser, P. D., and P. M. Bramley. 2004. The biosynthesis and nutritional uses of carotenoids. Prog. Lipid Res. 43:228-265.
13. Fraser, P. D., Y. Miura, and N. Misawa. 1997. In vitro characterization of astaxanthin biosynthetic enzymes. J. Biol. Chem. 272:6128-6135.
14. Fraser, P. D., S. Romer, C. A. Shipton, P. B. Mills, J. W. Kiano, N. Misawa, R. G. Drake, W. Schuch, and P. M. Bramley. 2002. Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc. Natl. Acad. Sci. USA 99:1092-1097.
15. Fraser, P. D., H. Shimada, and N. Misawa. 1998. Enzymic confirmation of reactions involved in routes to astaxanthin formation, elucidated using a direct substrate in vitro assay. Eur. J. Biochem. 252:229-236.
16. Giovannucci, E., A. Ascherio, E. B. Rimm, M. J. Stampfer, G. A. Colditz, and W. C. Willet. 1995. Intake of carotenids and retinol in relation to risk of prostate cancer. J. Natl. Cancer Inst. 87:1767-1776.
17. Hannibal, L., J. Lorquin, N. A. D'Ortoli, N. Garcia, C. Chaintreuil, C. Masson-Boivin, B. Dreyfus, and E. Giraud. 2000. Isolation and characterization of the canthaxanthin biosynthesis genes from the photosynthetic bacterium Bradyrhizobium sp. strain ORS278. J. Bacteriol. 182:3850-3853.
18. Higgins, D. G., J. D. Thompson, and T. J. Gibson. 1996. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266:383-402.
19. Bundle, B., M. Alberti, V. Nievelstein, P. Beyer, H. Kleinnig, G. A. Armstrong, D. H. Burke, and J. E. Hearst. 1994. Functional assignment of Erwinia herbicola Eho10 carotenoid genes expressed in Escherichia coli. Mol. Gen. Genet. 245:406-416.
20. Iwamoto, T., K. Hosoda, R. Hirano, H. Kurata, A. Matsumoto, W. Miki, M. Kamiyama, H. Itakura, S. Yamamoto, and K. Kondo. 2000. Inhibition of low-density lipoprotein oxidation by astaxanthin. J. Atheroscler. Thromb. 7:216-222.
21. Izumida, H., K. Adachi, M. Nishijima, M. Endo, and W. Miki. 1995. Akalone: a novel xanthin oxidase inhibitor produced by the marine bacterium, Agrobactcrium aurantiacum sp. nov. J. Mar. Biotchnol. 2:115-118.
22. Kuzuyama, T., and H. Seto. 2003. Diversity of the biosynthesis of the isoprene units. Nat. Prod. Rep. 20:171-183.
23. Larsen, R. A., M. M. Wilson, A. M. Guss, and W. W. Metcalf. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch. Microbiol. 178:193-201.
24. Mannisto, S., S. A. Smith-Warner, D. Spiegelman, D. Albanes, K. Anderson, P. A. van den Brandt, J. R. Cerhan, G. Colditz, D. Feskanich, J. L. Freudenheim, E. Giovannucci, R. A. Gohldbohm, S. Graham, et al. 2004. Dietary carotenoids and risk of lung cancer in a pooled analysis of seven cohort studies. Cancer Epidemiol. Biomarkers Prev. 13:40-48.
25. Matsumura, H., H. Takeyama, E. Husakabe, J. G. Burgess, and T. Matsunaga. 1997. Cloning, sequencing and expression the carotenoid biosynthesis gene, lycopene cyclase and phytoene desaturase, from the aerobic photosynthetic bacterium Erythrobacter longus strain Och 101 in Escherichia coli. Gene 189:169-174.
26. Matthews, P. D., and E. T. Wurtzel. 2000. Metabolic engineering of carotenoid accumulation in Escherichia coli by modulation of the isoprenoid precursor pool with expression of deoxyxylulose phosphate synthase. Appl. Microbiol. Biotechnol. 53:396-400.
27. Mayne, S. T. 1996. β-Carotene, carotenoids, and disease prevention in humans. FASEB J. 10:690-701.
28. Mazaffarieh, M., S. Sacu, and A. Wedrich. 2003. The role of the carotenoids, lutein and zeaxanthin, in protecting against age-related macular degeneration: a review based on controversial evidence. Nutr. J. 2:20.
29. Misawa, N., S. Kajiwara, K. Kondo, A. Yokoyama, Y. Satomi, T. Saito, W. Miki, and T. Ohtani. 1995. Canthaxanthin biosynthesis by the conversion of methylene to keto groups in a hydrocarbon β-carotene by a single gene. Biochem. Biophys. Res. Commun. 209:867-876.
30. Misawa, N., M. Nakagawa, K. Kobayashi, S. Yamano, Y. Izawa, K. Nakamura, and K. Harashima. 1990. Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J. Bacteriol. 172:6704-6712.
31. Misawa, N., Y. Satomi, K. Kondo, A. Yokoyama, S. Kajiwara, T. Saito, T. Ohtani, and W. Miki. 1995. Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J. Bacteriol. 177:6575-6584.
32. Misawa, N., and H. Shimada. 1998. Metabolic engineering for the production of carotenoids in non-carotenogenic bacteria and yeasts. J. Biotechnol. 59:169-181.
33. Miura, Y., K. Kondo, T. Saito, H. Shimada, P. D. Fraser, and N. Misawa. 1998. Production of the carotenoids lycopene, β-carotene, and astaxanthin in the food yeast Candida utilis. Appl. Environ. Microbiol. 64:1226-1229.
34. Nakagawa, M., and N. Misawa. 1991. Analysis of carotenoid glycosides produced in gram-negative bacteria by introduction of the Erwinia uredobora carotenoid biosynthesis genes. Agric. Biol. Chem. 55:2147-2148.
35. Nicholas, K. B., H. B. Nicholas, Jr., and D. W. Duel-field II. 1997. GeneDoc: analysis and visualization of genetic variation. Embnew. News 4:14.
36. Nishino, H., M. Murakoshi, T. Ii, M. Takemura, M. Kuchide, M. Kanazawa, X. Y. Mou, S. Wada, M. Masuda, Y. Ohsaka, S. Yogosawa, Y. Satomi, and K. Jinno. 2002. Carotenoids in cancer chemoprevention. Cancer Metastasis Rev. 21:257-264.
37. Pasamontes, L., D. Hug, M. Tessier, H. P. Hohmann, J. Schierle, and A. P. van Loon. 1997. Isolation and characterization of the carotenoid biosynthesis genes of Flavobacterium sp. strain R1534. Gene 185:35-41.
38. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
39. Sandmann, G. 2001. Carotenoid biosynthesis and biotechnological application. Arch. Biochem. Biophys. 385:4-12.
40. Sandmann, G. 2002. Combinatorial biosynthesis of carotenoids in a heterologous host: a powerful approach for the biosynthesis of novel structures. Chembiochem 3:629-635.
41. Sandmann, G., N. Misawa, M. Wiedemann, P. Vittorioso, A. Carattoli, G. Morelli, and G. Macino. 1993. Functional identification of al-3 from Neurospora crassa as the gene for geranylgeranyl pyrophosphate synthase by complementation with crt genes, in vitro characterization of the gene product and mutant analysis. J. Photochem. Photobiol. B 18:245-251.
42. Schmidt-Dannert, C. 2000. Engineering novel carotenoids in microorganisms. Curr. Opin. Biotechnol. 11:255-261.
43. Schmidt-Dannert, C., D. Umeno, and F. H. Arnold. 2000. Molecular breeding of carotenoid biosynthetic pathways. Nat. Biotechnol. 18:750-753.
44. Schnurr, G., A. Schmidt, and G. Sandmann. 1991. Mapping of a carotenogenic gene cluster from Erwinia herbicola and functional identification of six genes. FEMS Microbiol. Lett. 78:157-162.
45. Semba, R. D., and G. Dagnelie. 2003. Are lutein and zeaxanthin conditionally essential nutrients for eye health? Med. Hypotheses 61:465-472.
46. Shewmaker, C. K., J. A. Sheehy, M. Daley, S. Colburn, and D. Y. Ke. 1999. Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J. 20:401-412.
47. Shimada, H., K. Kondo, P. D. Fraser, Y. Miura, T. Saito, and N. Misawa. 1998. Increased carotenoid production by the food yeast Candida utilis through metabolic engineering of the isoprenoid pathway. Appl. Environ. Microbiol. 64:2676-2680.
48. Shindo, K., Y. Kagiyama, R. Nakamura, A. Hara, H. Ikenaga, K. Furukawa, and N. Misawa. 2003. Enzymatic synthesis of novel antioxidant flavonoids by Escherichia coli cells expressing modified metabolic genes involved in biphenyl catabolism. J. Mol. Catal. B 23:9-16.
49. Teramoto, M., S. Takaichi, Y. Inomata, H. Ikenaga, and N. Misawa. 2003. Structural and functional analysis of a lycopene β-monocyclase gene isolated from a unique marine bacterium that produces myxol. FEBS Lett. 545:120-126.
50. Umeno, D., and F. H. Arnold. 2003. A C35 carotenoid biosynthetic pathway. Appl. Environ. Microbiol. 69:3573-3579.
51. Vogt, T. M., S. T. Mayne, B. I. Graubard, C. A. Swanson, A. L. Sowell, J. B. Schoenber, G. M. Swanson, R. S. Greenberg, R. N. Hoover, R. B. Haynes, and R. G. Ziegler. 2002. Serum lycopene, other serum carotenoids, and risk of prostate cancer in US blacks and whites. Am. J. Epidemiol. 155:1023-1032.
52. Wang, C. W., M.-K. Oh, and J. C. Liao. 1999. Engineered isoprenoid pathway enhances astaxanthin production in Escherichia coli. Biotechnol. Bioeng. 62:235-241.
53. Yokoyama, A., K. Adachi, and Y. Shizuri. 1995. New carothenoid glycosides, astaxanthin glucoside and adonixanthin glucoside, isolated from the astaxanthin-producing marine bacterium, Agrobacterium aurantiacum. J. Nat. Prod. 58:1929-1933.
54. Yokoyama, A., H. Izumida, and Y. Shizuri. 1996. New carotenoid sulfates isolated from a marine bacterium. Biosci. Biotech. Biochem. 60:1877-1878.
55. Yokoyama, A., W. Miki, H. Izumida, and Y. Shizuri. 1996. New trihydroxyketo-carotenoids isolated from an astaxanthin-producing marine bacterium. Biosci. Biotech. Biochem. 60:200-203.
56. Yuan, J. M., D. O. Stram, K. Arakawa, H. P. Lee, and M. C. Yu. 2003. Dietary cryptoxanthin and reduced risk of lung cancer: the Singapore Chinese Health Study. Cancer Epidemiol. Biomarkers Prev. 12:890-898.