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Structural diversity and functional novelty of new carotenoid biosynthesis genes

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Journal of Industrial Microbiology and Biotechnology

Abstract

Many new carotenoid synthesis genes have recently been identified through genomic sequencing or functional cloning. Some of them exhibit novel structures and/or novel functions. This review describes such examples in the families of lycopene β-cyclases, putative homologues of phytoene dehydrogenases and new carotenoid hydroxylases. Both the functionally novel lycopene β-monocyclases and structurally novel fusion-type of lycopene β-cyclases were described. Another newly discovered sequence of lycopene β-cyclase described might represent a new class of lycopene β-cyclases previously not identified in several cyanobacteria. Three examples of putative homologues of phytoene dehydrogenases were described, however, they were confirmed to encode different and/or new functions such as β-carotene ketolase, 4,4′-diapolycopene oxygenase or prolycopene isomerase. Two new carotenoid hydroxylase genes were described that encoded the new function of 2,2′-β-ionone ring hydroxylase or 3,3′-isorenieratene hydroxylase. Phylogenetic analysis of these genes shed light on their possible evolutionary origins. These new genes also provide tools for synthesis of novel and desirable carotenoids by genetic engineering.

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References

  1. Alper H, Miyaoku K, Stephanopoulos G (2005) Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat Biotechnol 23:612–616

    Article  PubMed  CAS  Google Scholar 

  2. Armstrong G (1999) Carotenoid genetics and biochemistry. In: Cane DE (ed) Comprehensive natural products chemistry, vol 2. Elsevier, Oxford, pp 321–352

  3. Armstrong GA, Alberti M, Leach F, Hearst JE (1989) Nucleotide sequence, organization, and nature of the protein products of the carotenoid biosynthesis gene cluster of Rhodobacter capsulatus. Mol Gen Genet 216:254–268

    Article  PubMed  CAS  Google Scholar 

  4. Arrach N, Fernandez-Martin R, Cerda-Olmedo E, Avalos J (2001) A single gene for lycopene cyclase, phytoene synthase, and regulation of carotene biosynthesis in Phycomyces. Proc Natl Acad Sci USA 98:1687–1692

    Article  PubMed  CAS  Google Scholar 

  5. Arrach N, Schmidhauser TJ, Avalos J (2002) Mutants of the carotene cyclase domain of al-2 from Neurospora crassa. Mol Genet Genomics 266:914–921

    Article  PubMed  CAS  Google Scholar 

  6. Beyer P, Kroncke U, Nievelstein V (1991) On the mechanism of the lycopene isomerase/cyclase reaction in Narcissus pseudonarcissus L. chromoplasts. J Biol Chem 266:17072–17078

    PubMed  CAS  Google Scholar 

  7. Breitenbach J, Sandmann G (2005) zeta-Carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta 220:785–793

    Article  PubMed  CAS  Google Scholar 

  8. Breitenbach J, Vioque A, Sandmann G (2001) Gene sll0033 from Synechocystis 6803 encodes a carotene isomerase involved in the biosynthesis of all-E lycopene. Z Naturforsch [C] 56:915–917

    CAS  Google Scholar 

  9. Britton G, Liaaen-Jensen S, Pfander H (ed) (2004) Carotenoids handbook. Birkhauser Verlag, Basel

  10. Cunningham FX Jr, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613–1626

    Article  PubMed  CAS  Google Scholar 

  11. Cunningham FX Jr, Sun Z, Chamovitz D, Hirschberg J, Gantt E (1994) Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp strain PCC7942. Plant Cell 6:1107–1121

    Article  PubMed  CAS  Google Scholar 

  12. Dufosse L (2005) Brevibacterium aurantiacum, carotenogenic hydrox mutant: a unique source of isorenieratene, carotenoid now readily available for biological function assessment. Carotenoid Sci 9:135

    Google Scholar 

  13. Dufosse L, de Echanove C (2005) The last step in the biosynthesis of aryl carotenoids in the cheese ripening bacteria Brevibacterium linens ATCC9175 (Brevibacterium aurantiacum sp. Nov.) involves a cytochrome P450-dependent monooxygenase. Carotenoid Sci 9:136

    Google Scholar 

  14. Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA, Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514

    Article  PubMed  CAS  Google Scholar 

  15. Fernandez-Gonzalez B, Sandmann G, Vioque A (1997) A new type of asymmetrically acting beta-carotene ketolase is required for the synthesis of echinenone in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 272:9728–9733

    Article  PubMed  CAS  Google Scholar 

  16. Gari E, Toledo JC, Gibert I, Barbe J (1992) Nucleotide sequence of the methoxyneurosporene dehydrogenase gene from Rhodobacter sphaeroides: comparison with other bacterial carotenoid dehydrogenases. FEMS Microbiol Lett 72:103–108

    Article  PubMed  CAS  Google Scholar 

  17. Hannibal L, Lorquin J, D’Ortoli NA, Garcia N, Chaintreuil C, Masson-Boivin C, Dreyfus B, Giraud E (2000) Isolation and characterization of canthaxanthin biosynthesis genes from the photosynthetic bacterium Bradyrhizobium sp. strain ORS278. J Bacteriol 182:3850–3853

    Article  PubMed  CAS  Google Scholar 

  18. Hemmi H, Ikejiri S, Nakayama T, Nishino T (2003) Fusion-type lycopene beta-cyclase from a thermoacidophilic archaeon Sulfolobus solfataricus. Biochem Biophys Res Commun 305:586–591

    Article  PubMed  CAS  Google Scholar 

  19. Hugueney P, Badillo A, Chen HC, Klein A, Hirschberg J, Camara B, Kuntz M (1995) Metabolism of cyclic carotenoids: a model for the alteration of this biosynthetic pathway in Capsicum annuum chromoplasts. Plant J 8:417–424

    Article  PubMed  CAS  Google Scholar 

  20. Isaacson T, Ohad I, Beyer P, Hirschberg J (2004) Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol 136:4246–4255

    Article  PubMed  CAS  Google Scholar 

  21. Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 14:333–342

    Article  PubMed  CAS  Google Scholar 

  22. Kajiwara S, Kakizono T, Saito T, Kondo K, Ohtani T, Nishio N, Nagai S, Misawa N (1995) Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis, and astaxanthin synthesis in Escherichia coli. Plant Mol Biol 29:343–352

    Article  PubMed  CAS  Google Scholar 

  23. Krubasik P, Sandmann G (2000) A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol Gen Genet 263:423–432

    Article  PubMed  CAS  Google Scholar 

  24. Krubasik P, Sandmann G (2000) Molecular evolution of lycopene cyclases involved in the formation of carotenoids with ionone end groups. Biochem Soc Trans 28:806–810

    Article  PubMed  CAS  Google Scholar 

  25. Krugel H, Krubasik P, Weber K, Saluz HP, Sandmann G (1999) Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim Biophys Acta 1439:57–64

    PubMed  CAS  Google Scholar 

  26. Liaaen-Jensen S, Hegge E, Jackman LM (1964) Bacterial Carotenoids: The carotenoids of photosynthetic green bacteria. Acta Chem Scand 18:1703–1718

    Article  Google Scholar 

  27. Linden H, Misawa N, Saito T, Sandmann G (1994) A novel carotenoid biosynthesis gene coding for zeta-carotene desaturase: functional expression, sequence and phylogenetic origin. Plant Mol Biol 24:369–379

    Article  PubMed  CAS  Google Scholar 

  28. Maresca JA, Frigaard NU, Bryant DA (2005) Identification of a novel class of lycopene cyclases in photosynthetic organisms. Allen Press, Canada

    Google Scholar 

  29. Masamoto K, Wada H, Kaneko T, Takaichi S (2001) Identification of a gene required for cis-to-trans carotene isomerization in carotenogenesis of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 42:1398–1402

    Article  PubMed  CAS  Google Scholar 

  30. Mijts BN, Lee PC, Schmidt-Dannert C (2005) Identification of a carotenoid oxygenase synthesizing acyclic xanthophylls: combinatorial biosynthesis and directed evolution. Chem Biol 12:453–460

    Article  PubMed  CAS  Google Scholar 

  31. Misawa N, Satomi Y, Kondo K, Yokoyama A, Kajiwara S, Saito T, Ohtani T, Miki W (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

    PubMed  CAS  Google Scholar 

  32. Mochimaru M, Masukawa H, Takaichi S (2005) The cyanobacterium Anabaena sp. PCC 7120 has two distinct beta-carotene ketolases: CrtO for echinenone and CrtW for ketomyxol synthesis. FEBS Lett 579:6111–6114

    Article  PubMed  CAS  Google Scholar 

  33. Nishida Y, Adachi K, Kasai H, Shizuri Y, Shindo K, Sawabe A, Komemushi S, Miki W, Misawa N (2005) Elucidation of a carotenoid biosynthesis gene cluster encoding a novel enzyme, 2,2′-{beta}-hydroxylase, from Brevundimonas sp. strain SD212 and combinatorial biosynthesis of new or rare xanthophylls. Appl Environ Microbiol 71:4286–44296

    Article  PubMed  CAS  Google Scholar 

  34. Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332

    Article  PubMed  CAS  Google Scholar 

  35. Pasamontes L, Hug D, Tessier M, Hohmann HP, Schierle J, van Loon AP (1997) Isolation and characterization of the carotenoid biosynthesis genes of Flavobacterium sp. strain R1534. Gene 185:35–41

    Article  PubMed  CAS  Google Scholar 

  36. Peck RF, Johnson EA, Krebs MP (2002) Identification of a lycopene beta-cyclase required for bacteriorhodopsin biogenesis in the archaeon Halobacterium salinarum. J Bacteriol 184:2889–2897

    Article  PubMed  CAS  Google Scholar 

  37. Pecker I, Gabbay R, Cunningham FX Jr, Hirschberg J (1996) Cloning and characterization of the cDNA for lycopene beta-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol Biol 30:807–819

    Article  PubMed  CAS  Google Scholar 

  38. Sandmann G (1994) Phytoene desaturase: genes, enzymes and phylogenetic aspects. J Plant Physiol 143:444–447

    CAS  Google Scholar 

  39. Schnurr G, Misawa N, Sandmann G (1996) Expression, purification and properties of lycopene cyclase from Erwinia uredovora. Biochem J 315(Pt 3):869–874

    PubMed  CAS  Google Scholar 

  40. Takaichi S, Wang ZY, Umetsu M, Nozawa T, Shimada K, Madigan MT (1997) New carotenoids from the thermophilic green sulfur bacterium Chlorobium tepidum: 1′,2′-dihydro-gamma-carotene, 1′,2′-dihydrochlorobactene, and OH-chlorobactene glucoside ester, and the carotenoid composition of different strains. Arch Microbiol 168:270–276

    Article  PubMed  CAS  Google Scholar 

  41. Tao L, Cheng Q (2004) Novel β-carotene ketolases from non-photosynthetic bacteria for canthaxanthin synthesis. Mol Gen Genomics 272:530–537

    Article  CAS  Google Scholar 

  42. Tao L, Picataggio S, Rouviere PE, Cheng Q (2004) Asymmetrically acting lycopene β-cyclases (CrtLm) from non-photosynthetic bacteria. Mol Gen Genomics 271:180–188

    Article  CAS  Google Scholar 

  43. Tao L, Schenzle A, Odom JM, Cheng Q (2005) Novel carotenoid oxidase involved in biosynthesis of 4,4′-diapolycopene dialdehyde. Appl Environ Microbiol 71:3294–3301

    Article  PubMed  CAS  Google Scholar 

  44. Teramoto M, Takaichi S, Inomata Y, Ikenaga H, Misawa N (2003) Structural and functional analysis of a lycopene beta-monocyclase gene isolated from a unique marine bacterium that produces myxol. FEBS Lett 545:120–126

    Article  PubMed  CAS  Google Scholar 

  45. Velayos A, Eslava AP, Iturriaga EA (2000) A bifunctional enzyme with lycopene cyclase and phytoene synthase activities is encoded by the carRP gene of Mucor circinelloides. Eur J Biochem 267:5509–5519

    Article  PubMed  CAS  Google Scholar 

  46. Verdoes JC, Krubasik KP, Sandmann G, van Ooyen AJ (1999) Isolation and functional characterisation of a novel type of carotenoid biosynthetic gene from Xanthophyllomyces dendrorhous. Mol Gen Genet 262:453–461

    Article  PubMed  CAS  Google Scholar 

  47. Viveiros M, Krubasik P, Sandmann G, Houssaini-Iraqui M (2000) Structural and functional analysis of the gene cluster encoding carotenoid biosynthesis in Mycobacterium aurum A+. FEMS Microbiol Lett 187:95–101

    Article  PubMed  CAS  Google Scholar 

  48. Wieland B, Feil C, Gloria-Maercker E, Thumm G, Lechner M, Bravo JM, Poralla K, Gotz F (1994) Genetic and biochemical analyses of the biosynthesis of the yellow carotenoid 4,4′-diaponeurosporene of Staphylococcus aureus. J Bacteriol 176:7719–7726

    PubMed  CAS  Google Scholar 

  49. Yokoyama A, Izumida H, Shizuri Y (1996) New carotenoid sulfates isolated from a marine bacterium. Biosci Biotechnol Biochem 60:1877–1878

    Article  Google Scholar 

  50. Yokoyama A, Miki W, Izumida H, Shizuri Y (1996) New trihydroxy-keto-carotenoids isolated from an astaxanthin-producing marine bacterium. Biosci Biotech Biochem 60:200–203

    CAS  Google Scholar 

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  1. Biological and Chemical Sciences and Engineering, Central Research and Development, E. I. DuPont de Nemours Inc., Experimental Station, E328/B48, Wilmington, DE, 19880-0328, USA

    Qiong Cheng

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Cheng, Q. Structural diversity and functional novelty of new carotenoid biosynthesis genes. J IND MICROBIOL BIOTECHNOL 33, 552–559 (2006). https://doi.org/10.1007/s10295-006-0121-4

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  • DOI: https://doi.org/10.1007/s10295-006-0121-4

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