Carotenoid β-ring hydroxylase and ketolase from marine bacteria - Promiscuous enzymes for synthesizing functional xanthophylls

Marine Drugs

Volumn 9, Issue 5, 2011, Pages 757-771

  Misawa, Norihiko ^a  

^a ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

Author keywords

Brevundimonas; Functional xanthophyll; Ketocarotenoid; Marine bacteria; Paracoccus

Indexed keywords

CAROTENOID 2,2 HYDROXYLASE; CAROTENOID 3,3' HYDROXYLASE; CAROTENOID 4,4' KETOLASE; OXYGENASE; UNCLASSIFIED DRUG; XANTHOPHYLL;

ALPHAPROTEOBACTERIA; BACTERIAL GENE; BIOSYNTHESIS; CAROTENOID 2,2 HYDROXYLASE GENE; CAROTENOID 3,3' HYDROXYLASE GENE; CAROTENOID 4,4' KETOLASE GENE; ESCHERICHIA COLI; GENE CLUSTER; GENE EXPRESSION; GENE SEQUENCE; GENETIC ENGINEERING; MARINE BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; REVIEW; SIGNAL TRANSDUCTION; VITAMIN METABOLISM;

ALPHAPROTEOBACTERIA; BREVUNDIMONAS; ESCHERICHIA COLI; PARACOCCUS (BACTERIUM);

EID: 79957660778     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md9050757     Document Type: Review

References (75)

1. Britton, G.; Liaaen-Jensen, S.; Pfander, H. Carotenoids Handbook; Birkhauser Verlag: Basel, Switzerland, 2004.
2. Shindo, K.; Endo, M.; Miyake, Y.; Wakasugi, K.; Morritt, D.; Bramley, P.M.; Fraser, P.D.; Kasai, H.; Misawa, N. Methyl glucosyl-3,4-dehydro-apo- 8′-lycopenoate, a novel antioxidative glyco-C30-carotenoic acid produced by a marine bacterium Planococcus maritimus. J. Antibiot. 2008, 61, 729-735.
3. 30-carotenoic acid produced by a new marine bacterium Rubritalea squalenifaciens. Tetrahedron Lett. 2007, 48, 2725-2727.
4. Tao, L.; Yao, H.; Kasai, H.; Misawa, N.; Cheng, Q. A carotenoid synthesis gene cluster from Algoriphagus sp. KK10202C with a novel fusion-type lycopene-β-cyclase gene. Mol. Genet. Genomics 2006, 276, 79-86.
5. Shindo, K.; Kikuta, K.; Suzuki, A.; Katsuta, A.; Kasai, H.; Yasumoto-Hirose, M.; Matuo, Y.; Misawa, N.; Takaichi, S. Rare carotenoids, (3R)-Saproxanthin and (3R,2′S)-myxol, isolated from novel marine bacteria (Flavobacteriaceae) and their antioxidant activities. Appl. Microbiol. Biotechnol. 2007, 74, 1350-1357.
6. Teramoto, M.; Takaichi, S.; Inomata, Y.; Ikenaga, H.; Misawa, N. Structural and functional analysis of a lycopene β-monocyclase gene isolated from a unique marine bacterium that produces myxol. FEBS Lett. 2003, 545, 120-126.
7. Yokoyama, A.; Izumida, H.; Miki, W. Production of astaxanthin and 4-ketozeaxanthin by the marine bacterium, Agrobacterium aurantiacum. Biosci. Biotechnol. Biochem. 1994, 58, 1842-1844.
8. Yokoyama, A.; Izumida, H.; Shizuri, Y. New carotenoid sulfates isolated from a marine bacterium. Biosci. Biotechnol. Biochem. 1996, 60, 1877-1878.
9. Yokoyama, A.; Miki, W.; Izumida, H.; Shizuri, Y. New trihydroxy-keto- carotenoids isolated from an astaxanthin-producing marine bacterium. Biosci. Biotechnol. Biochem. 1996, 60, 200-203.
10. Maruyama, T.; Kasai, H.; Choi, S.K.; Ramasamy, A.K.; Inomata, Y.; Misawa, N. Structure of a complete carotenoid biosynthesis gene cluster of marine bacterium Paracoccus sp. strain N81106. Carotenoid Sci. 2007, 11, 50-55.
11. Nishida, Y.; Adachi, K.; Kasai, H.; Shizuri, Y.; Shindo, K.; Sawabe, A.; Komemushi, S.; Miki, W.; Misawa, N. 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. Appl. Environ. Microbiol. 2005, 71, 4286-4296.
12. Nishino, H.; Murakoshi, M.; Ii, T.; Takemura, M.; Kuchide, M.; Kanazawa, M.; Mou, X.Y.; Wada, S.; Masuda, M.; Ohsaka, Y.; et al. Carotenoids in cancer chemoprevention. Cancer Metastasis Rev. 2002, 21, 257-264.
13. Pashkow, F.J.; Watumull, D.G.; Campbell, C.L. Astaxanthin: A novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am. J. Cardiol. 2008, 101, 58D-68D.
14. Camera, E.; Matrofrancesco, A.; Fabbri, C.; Daubrawa, F.; Picardo, M.; Sies, H.; Stahl, W. Astaxanthin, canthaxanthin and β-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes. Exp. Dermatol. 2009, 18, 222-231.
15. Jackson, H.; Braun, C.L.; Ernst, H. The chemistry of novel xanthophyll carotenoids. Am. J. Cardiol. 2008, 101, 50D-57D.
16. Misawa, N. Pathway engineering of plants toward astaxanthin production. Plant Biotechnol. 2009, 26, 93-99.
17. Izumida, H.; Adachi, K.; Nishizima, M.; Endo, M.; Miki, W. Akalone: A novel xanthine oxidase inhibitor produced by the marine bacterium, Agrobacterium aurantiacum sp. nov. J. Mar. Biotechnol. 1995, 2, 115-118.
18. Yokoyama, A.; Adachi, K.; Shizuri, Y. New carotenoid glycosides, astaxanthin glucoside and adonixanthin glucoside, isolated from the astaxanthin-producing marine bacterium, Agrobacterium aurantiacum. J. Nat. Prod. 1995, 58, 1929-1933.
19. Lee, J.H.; Kim, Y.S.; Choi, T.J.; Lee, W.J.; Kim, Y.T. Paracoccus haeundaensis sp. nov., a Gram-negative, halophilic, astaxanthin-producing bacterium. Int. J. Syst. Evol. Microbiol. 2004, 54, 1699-1672.
20. T is adonixanthin diglucoside. J. Nat. Prod. 2006, 69, 1823-1825.
21. Khan, S.T.; Takaichi, S.; Harayama, S. Paracoccus marinus sp. nov., an adonixanthin diglucoside-producing bacterium isolated from coastal seawater in Tokyo Bay. Int. J. Syst. Evol. Microbiol. 2008, 58, 383-386.
22. Harker, M.; Hirschberg, J.; Oren, A. Paracoccus marcusii sp. nov., an orange gram-negative coccus. Int. J. Syst. Bacteriol. 1998, 48, 543-548.
23. Misawa, N.; Nakagawa, M.; Kobayashi, K.; Yamano, S.; Izawa, Y.; Nakamura, K.; Harashima, K. Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J. Bacteriol. 1990, 172, 6704-6712.
24. Armstrong, G.A.; Alberti, M.; Hearst, J.E. Conserved enzymes mediate the early reactions of carotenoid biosynthesis in nonphotosynthetic and photosynthetic prokaryotes. Proc. Natl. Acad. Sci. USA 1990, 87, 9975-9979.
25. Hundle, B.S.; Beyer, P.; Kleinig, H.; Englert, G.; Hearst, J.E. Carotenoids of Erwinia herbicola and an Escherichia coli HB101 strain carrying the Erwinia herbicola carotenoid gene cluster. Photochem. Photobiol. 1991, 54, 89-93.
26. Nakagawa, M.; Misawa, N. Analysis of carotenoid glycosides produced in gram-negative bacteria by introduction of the Erwinia uredovora carotenoid biosynthesis genes. Agric. Biol. Chem. 1991, 55, 2147-2148.
27. Sandmann, G.; Misawa, N. New functional assignment of the carotenogenic genes crtB and crtE with constructs of these genes from Erwinia species. FEMS Microbiol. Lett. 1992, 90, 253-258.
28. Math, S.K.; Hearst, J.E.; Poulter, C.D. The crtE gene in Erwinia herbicola encodes geranylgeranyl diphosphate synthase. Proc. Natl. Acad. Sci. USA 1992, 89, 6761-6764.
29. Neudert, U.; Martines-Ferez, I.M.; Fraser, P.D.; Sandmann, G. Expression of an active phytoene synthease from Erwinia uredovora and biochemical properties of the enzyme. Biochim. Biophys. Acta 1998, 1392, 51-58.
30. Fraser, P.D.; Misawa, N.; Linden, H.; Yamano, S.; Kobayashi, K.; Sandmann, G. Expression in E. coli, purification and reactivation of the recombinant Erwinia uredovora phytoene desturase. J. Biol. Chem. 1992, 267, 19891-19895.
31. Schnurr, G.; Misawa, N.; Sandmann, G. Expression, purification and properties of lycopene cyclase from Erwinia uredovora. Biochem. J. 1996, 315, 869-874.
32. Hundle, B.S.; O'Brien, D.A.; Alberti, M.; Beyer, P.; Hearst, J.E. Functional expression of zeaxanthin glucosyltransferase from Erwinia herbicola and a proposed uridine diphosphate binding site. Proc. Natl. Acad. Sci. USA 1992, 89, 9321-9325.
33. Misawa, N.; Kajiwara, S.; Kondo, K.; Yokoyama, A.; Satomi, Y.; Saito, T.; Miki, W.; Ohtani, T. Canthaxanthin biosynthesis by the conversion of methylene to keto groups in a hydrocarbon β-carotene by a single gene. Biochem. Biophy. Res. Commun. 1995, 209, 867-876.
34. Misawa, N.; Truesdale, M.R.; Sandmann, G.; Fraser, P.D.; Bird, C.; Schuch, W.; Bramley, P.M. Expression of a tomato cDNA coding for phytoene synthase in Escherichia coli, phytoene formation in vivo and in vitro, and functional analysis of the various truncated gene products. J. Biochem. 1994, 116, 980-985. (Pubitemid 24354644)
35. Misawa, N.; Satomi, Y.; Kondo, K.; Yokoyama, A.; Kajiwara, S.; Saito, T.; Ohtani, T.; Miki, W. Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J. Bacteriol. 1995, 177, 6575-6584.
36. Sun, Z.; Gantt, E.; Cunningham, F.X., Jr. Cloning and functional analysis of the β-carotene hydroxylase of Arabidopsis thaliana. J. Biol. Chem. 1996, 271, 24349-24352.
37. Hannibal, L.; Lorquin, J.; D'Ortoli, N.A.; Garcia, N.; Chaintreuil, C.; Masson-Boivin, C.; Dreyfus, B.; Giraud, E. Isolation and characterization of the canthaxanthin biosynthesis genes from the photosynthetic bacterium Bradyrhizobium sp. strain ORS278. J. Bacteriol. 2000, 182, 3850-3853.
38. Kaneda, K.; Kuzuyama, T.; Takagi, M.; Hayakawa, Y.; Seto, H. An unusual isopentenyl diphosphate isomerase found in the mevalonate pathway gene cluster from Streptomyces sp. strain CL190. Proc. Natl. Acad. Sci. USA 2001, 98, 932-937.
39. Misawa, N. Carotenoids. In Comprehensive Natural Products II Chemistry and Biology; Mander, L., Lui, H.W., Eds.; Elsevier: Oxford, UK, 2010; Volume 1, pp. 733-753.
40. Ye, R.W.; Stead, K.J.; Yao, H.; He, H. Mutational and functional analysis of the β-carotene ketolase involved in the production of canthaxanthin and astaxanthin. Appl. Environ. Microbiol. 2006, 72, 5829-5837.
41. Sieiro, C.; Poza, M.; de Miguel, T.; Villa, T.G. Genetic basis of microbial carotenogenesis. Int. Microbiol. 2003, 6, 11-16.
42. Fraser, P.D.; Miura, Y.; Misawa, N. In vitro characterization of astaxanthin biosynthetic enzymes. J. Biol. Chem. 1997, 272, 6128-6135.
43. Fraser, P.D.; Shimada, H.; Misawa, N. Enzymic confirmation of reactions involved in routes to astaxanthin formation, elucidated using a direct substrate in vitro assay. Eur. J. Biochem. 1998, 252, 229-236.
44. Choi, S.K.; Nishida, Y.; Matsuda, S.; Adachi, K.; Kasai, H.; Peng, X.; Komemushi, S.; Miki, W.; Misawa, N. Characterization of β-carotene ketolases, CrtW, from marine bacteria by complementation analysis in Escherichia coli. Mar. Biotechnol. 2005, 7, 515-522.
45. Choi, S.K.; Matsuda, S.; Hoshino, T.; Peng, X.; Misawa, N. Characterization of bacterial β-carotene 3,3′-hydroxylases, CrtZ, and P450 in astaxanthin biosynthetic pathway and adonirubin production by gene combination in Escherichia coli. Appl. Microbiol. Biotechnol. 2006, 72, 1238-1246.
46. Makino, T.; Harada, H.; Ikenaga, H.; Matsuda, S.; Takaichi, S.; Shindo, K.; Sandmann, G.; Ogata, T.; Misawa, N. Characterization of cyanobacterial carotenoid ketolase CrtW and hydroxylase CrtR by complementation analysis in Escherichia coli. Plant Cell Physiol. 2008, 49, 1867-1878.
47. Steiger, S.; Sandmann, G. Cloning of two carotenid ketolase genes from Nostoc punctiforme for the heterologous production of canthaxanthin and astaxanthin. Biotechnol. Lett. 2004, 26, 813-817.
48. Mochimaru, M.; Masukawa, H.; Takaichi, S. The cyanobacterium Anabaena sp. PCC 7120 has two distinct β-carotene ketolases: CrtO for echinenone and CrtW for ketomyxol synthesis. FEBS Lett. 2005, 579, 6111-6114.
49. Takaichi, S.; Mochimaru, M.; Maoka, T.; Katoh, H. Myxol and 4-ketomyxol 2′-fucosides, not rhamnosides, from Anabaena sp. PCC 7120 and Nostoc punctiforme PCC 73102, and proposal for the biosynthetic pathway of carotenoids. Plant Cell Physiol. 2005, 46, 497-504.
50. Kajiwara, S.; Kakizono, T.; Saito, T.; Kondo, K.; Ohtani, T.; Nishio, N.; Nagai, S.; Misawa, N. Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis, and astaxanthin synthesis in Escherichia coli. Plant Mol. Biol. 1995, 29, 343-352.
51. Lotan, T.; Hirschberg, J. Cloning and expression in Escherichia coli of the gene encoding β-C-4-oxygenase, that converts β-carotene to the ketocarotenoid canthaxanthin in Haematococcus pluvialis. FEBS Lett. 1995, 364, 125-128.
52. Huang, J.C.; Chen, F.; Sandmann, G. Stress-related differential expression of multiple β-carotene ketolase genes in the unicellular green alga Haematococcus pluvialis. J. Biotechnol. 2006, 122, 176-185.
53. Giuliano, G.; Tavazza, R.; Diretto, G.; Beyer, P.; Taylor, M.A. Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol. 2008, 26, 139-145.
54. Fernandez-Gonzalez, B.; Sandmann, G.; Vioque, A. A new type of asymmetrically acting β-carotene ketolase is required for the synthesis of echinenone in the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 1997, 272, 9728-9733.
55. Takaichi, S.; Maoka, T.; Masamoto, K. Myxoxanthophyll in Synechocyctis sp. PCC 6803 is myxol 2′-dimethyl-fucoside, (3R,2′S)-myxol 2′-(2,4-di-O-methyl-α-L-fucoside), not rhamnoside. Plant Cell Physiol. 2001, 42, 756-762.
56. Tao, L.; Cheng, Q. Novel β-carotene ketolases from non-photosynthetic bacteria for canthaxanthin synthesis. Mol. Genet. Genomics 2004, 272, 530-537.
57. Choi, S.K.; Harada, H.; Matsuda, S.; Misawa, N. Characterization of two β-carotene ketolases, CrtO and CrtW, by complementation analysis in Escherichia coli. Appl. Microbiol. Biotechnol. 2007, 75, 1335-1341.
58. Masamoto, K.; Misawa, N.; Kaneko, T.; Kikuno, R.; Toh, H. β-carotene hydroxylase gene from the cyanobacterium Synechocystis sp. strain PCC6803. Plant Cell Physiol. 1998, 39, 560-564. (Pubitemid 28266031)
59. Takaichi, S.; Mochimaru, M. Carotenoids and carotenogenesis in cyanobacteria: Unique ketocarotenoids and carotenoid glycosides. Cell. Mol. Life Sci. 2007, 64, 2607-2619.
60. Mochimaru, M.; Masukawa, H.; Maoka, T.; Mohamed, H.E.; Vermaas, W.L.; Takaichi, S. Substrate specificities and availability of fucosyltransferase and β-carotene hydroxylase for myxol 2′-fucoside synthesis in Anabaena sp. strain PCC 7120 compared with Synechocystis sp. strain PCC 6803. J. Bacteriol. 2008, 190, 6726-6733.
61. Blasco, F.; Kauffmann, I.; Schmid, R.D. CYP175A1 from Thermus thermophilus HB27, the first β-carotene hydroxylase of the P450 superfamily. Appl. Microbiol. Biotechnol. 2004, 64, 671-674.
62. Tao, L.; Rouvière, P.E.; Cheng, Q. A carotenoid synthesis gene cluster from a non-marine Brevundimonas that synthesizes hydroxylated astaxanthin. Gene 2006, 379, 101-408.
63. Iwai, M.; Maoka, T.; Ikeuchi, M.; Takaichi, S. 2,2′-β- Hydroxylase (CrtG) is involved in carotenogenesis of both nostoxanthin and 2-hydroxymyxol 2′-fucoside in Thermosynechococcus elongatus strain BP-1. Plant Cell Physiol. 2008, 49, 1678-1687.
64. Osawa, A.; Harada, H.; Choi, S.K.; Misawa, N.; Shindo, K. Production of caloxanthin 3′-β-D-glucoside, zeaxanthin 3,3′-β-D- diglucoside, and nostoxanthin in a recombinant Escherichia coli expressing system harboring seven carotenoid biosynthesis genes, including crtX and crtG. Phytochemistry 2011, 72, 711-716.
65. Yokoyama, A.; Shizuri, Y.; Misawa, N. Production of new carotenoids, astaxanthin glucosides, by Escherichia coli transformants carrying carotenoid biosynthetic genes. Tetrahedron Lett. 1998, 39, 3709-3712. (Pubitemid 28222454)
66. Harada, H.; Misawa, N. Novel approaches and achievements in biosynthesis of functional isoprenoids in Escherichia coli. Appl. Microbiol. Biotechnol. 2009, 84, 1021-1031.
67. Misawa, N. Pathway engineering for functional isoprenoids. Curr. Opin. Biotechnol. 2011, doi:10.1016/j.copbio.2011.01.002.
68. Kajiwara, S.; Fraser, P.D.; Kondo, K.; Misawa, N. Expression of an exogenous isopentenyl diphosphate isomerase gene enhances isoprenoid biosynthesis in Escherichia coli. Biochem. J. 1997, 324, 421-426. (Pubitemid 27267983)
69. Harada, H.; Yu, F.; Okamoto, S.; Kuzuyama, T.; Utsumi, R.; Misawa, N. Efficient synthesis of functional isoprenoids from acetoacetate through metabolic pathway-engineered Escherichia coli. Appl. Microbiol. Biotechnol. 2009, 81, 915-925.
70. Kakinuma, K.; Dekishima, Y.; Matsushima, Y.; Eguchi, T.; Misawa, N.; Takagi, M.; Kuzuyama, T.; Seto, H. New approach to multiply deuterated isoprenoids using triply engineered Escherichia coli and its potential as a tool for mechanistic enzymology. J. Am. Chem. Soc. 2001, 123, 1238-1239.
71. Newman, J.D.; Marshall, J.; Chang, M.; Nowroozi, F.; Paradise, E.; Pitera, D.; Newman, K.L.; Keasling, J.D. High-level production of amorpha-4,11-diene in a two-phase partitioning bioreactor of metabolically engineered Escherichia coli. Biotechnol. Bioeng. 2006, 95, 684-691.
72. Vadali, R.V.; Fu, Y.; Bennett, G.N.; San, K.Y. Enhanced lycopene productivity by manipulation of carbon flow to isopentenyl diphosphate in Escherichia coli. Biotechnol. Prog. 2005, 21, 1558-1561.
73. Yoon, S.H.; Lee, Y.M.; Kim, J.E.; Lee, S.H.; Lee, J.H.; Kim, J.Y.; Jung, K.H.; Shin, Y.C.; Keasling, J.D.; Kim, S.W. Enhanced lycopene production in Escherichia coli engineered to synthesize isopentenyl diphosphate and dimethylallyl diphosphate from mevalonate. Biotechnol. Bioeng. 2006, 94, 1025-1032.
74. Alper, H.; Stephanopoulos, G. Uncovering the gene knockout landscape for improved lycopene production in E. coli. Appl. Microbiol. Biotechnol. 2008, 78, 801-810.
75. Hasunuma, T.; Miyazawa, S.; Yoshimura, S.; Shinzaki, Y.; Tomizawa, K.; Shindo, K.; Choi, S.K.; Misawa, N.; Miyake, C. Biosynthesis of astaxanthin in tobacco leaves by transplastomic engineering. Plant J. 2008, 55, 857-868.