1887

Abstract

The phytoene-related desaturases are the key enzymes in the carotenoid biosynthetic pathway. The gene encoding phytoene desaturase in the deinoxanthin synthesis pathway of was identified and characterized. Two putative phytoene desaturase homologues (DR0861 and DR0810) were identified by analysis of conserved amino acid regions, and the former displayed the highest identity (68 %) with phytoene desaturase of the cyanobacterium . DR0861 gene knockout and dinucleotide-binding motif deletion resulted in the arrest of lycopene synthesis and the accumulation of phytoene. The colourless DR0861 knockout mutant became more sensitive to acute ionizing radiation and oxygen stress. Complementation of the mutant with a heterologous or homologous gene restored its pigment and resistance. The desaturase activity of DR0861 () was further confirmed by the assay of enzyme activity and heterologous expression in containing and genes (responsible for phytoene synthesis) from . In addition, the amount of lycopene synthesis in resulting from the expression of from was determined, and this had significant dose-dependent effects on the survival rate of exposed to hydrogen peroxide and ionizing radiation.

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2007-05-01
2024-03-28
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References

  1. Armstrong G. A., Hearst J. E. 1996; Carotenoids 2: genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J 10:228–237
    [Google Scholar]
  2. Armstrong G. A., Alberti M., Leach F., Hearst J. E. 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 [CrossRef]
    [Google Scholar]
  3. Armstrong G. A., Alberti M., Hearst J. E. 1990; Conserved enzymes mediate the early reactions of carotenoid biosynthesis in nonphotosynthetic and photosynthetic prokaryotes. Proc Natl Acad Sci U S A 87:9975–9979 [CrossRef]
    [Google Scholar]
  4. Bartley G. E., Schmidhauser T. J., Yanofsky C., Scolnik P. A. 1990; Carotenoid desaturases from Rhodobacter capsulatus and Neurospora crassa are structurally and functionally conserved and contain domains homologous to flavoprotein disulfide oxidoreductases. J Biol Chem 265:16020–16024
    [Google Scholar]
  5. Carbonneau M. A., Melin A. M., Perromat A., Clerc M. 1989; The action of free radicals on Deinococcus radiodurans carotenoids. Arch Biochem Biophys 275:244–251 [CrossRef]
    [Google Scholar]
  6. Cox M. M., Battista J. R. 2005; Deinococcus radiodurans – the consummate survivor. Nat Rev Microbiol 3:882–892 [CrossRef]
    [Google Scholar]
  7. Daly M. J., Gaidamakova E. K., Matrosova V. Y., Vasilenko A., Zhai M., Venkateswaran A., Hess M., Omelchenko M. V., Kostandarithes H. M. other authors 2004; Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025–1028 [CrossRef]
    [Google Scholar]
  8. Earl A. M., Mohundro M. M., Mian I. S., Battista J. R. 2002; The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression. J Bacteriol 184:6216–6224 [CrossRef]
    [Google Scholar]
  9. Ehrenshaft M., Daub M. E. 1994; Isolation, sequence, and characterization of the Cercospora nicotianae phytoene dehydrogenase gene. Appl Environ Microbiol 60:2766–2771
    [Google Scholar]
  10. Fraser P. D., Misawa N., Linden H., Yamano S., Kobayashi K., Sandmann G. 1992; Expression in Escherichia coli , purification, and reactivation of the recombinant Erwinia uredovora phytoene desaturase. J Biol Chem 267:19891–19895
    [Google Scholar]
  11. Funayama T., Narumi I., Kikuchi M., Kitayama S., Watanabe H., Yamamoto K. 1999; Identification and disruption analysis of the recN gene in the extremely radioresistant bacterium Deinococcus radiodurans. Mutat Res 435:151–161 [CrossRef]
    [Google Scholar]
  12. Gao G., Lu H., Huang L., Hua Y. 2005; Construction of DNA damage response gene pprI function deficient and function complementary mutants in Deinococcus radiodurans. Chin Sci Bull 50:311–316
    [Google Scholar]
  13. Ghosal D., Omelchenko M. V., Gaidamakova E. K., Matrosova V. Y., Vasilenko A., Venkateswaran A., Zhai M., Kostandarithes H. M., Brim H. other authors 2005; How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol Rev 29:361–375
    [Google Scholar]
  14. Glaeser J., Klug G. 2005; Photo-oxidative stress in Rhodobacter sphaeroides : protective role of carotenoids and expression of selected genes. Microbiology 151:1927–1938 [CrossRef]
    [Google Scholar]
  15. Harada J., Nagashima K. V., Takaichi S., Misawa N., Matsuura K., Shimada K. 2001; Phytoene desaturase, CrtI, of the purple photosynthetic bacterium, Rubrivivax gelatinosus , produces both neurosporene and lycopene. Plant Cell Physiol 42:1112–1118 [CrossRef]
    [Google Scholar]
  16. Hua Y., Narumi I., Gao G., Tian B., Satoh K., Kitayama S., Shen B. 2003; PprI: a general switch responsible for extreme radioresistance of Deinococcus radiodurans. Biochem Biophys Res Commun 306:354–360 [CrossRef]
    [Google Scholar]
  17. Khairnar N. P., Misra H. S., Apte S. K. 2003; Pyrroloquinoline-quinone synthesized in Escherichia coli by pyrroloquinoline-quinone synthase of Deinococcus radiodurans plays a role beyond mineral phosphate solubilization. Biochem Biophys Res Commun 312:303–308 [CrossRef]
    [Google Scholar]
  18. Kitayama S., Asaka S., Totsuka K. 1983; DNA double-strand breakage and removal of cross-links in Deinococcus radiodurans. J Bacteriol 155:1200–1207
    [Google Scholar]
  19. Konola J. T., Sargent K. E., Gow J. B. 2000; Efficient repair of hydrogen peroxide-induced DNA damage by Escherichia coli requires SOS induction of RecA and RuvA proteins. Mutat Res 459:187–194 [CrossRef]
    [Google Scholar]
  20. Laurant L., Evelyne P., Michel C. 1997; Deinoxanthin: a new carotenoid isolated from Deinococcus radiodurans. Tetrahedron 53:919–926 [CrossRef]
    [Google Scholar]
  21. 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 [CrossRef]
    [Google Scholar]
  22. Lowe G. M., Booth L. A., Young A. J., Bilton R. F. 1999; Lycopene and beta-carotene protect against oxidative damage in HT29 cells at low concentrations but rapidly lose this capacity at higher doses. Free Radic Res 30:141–151 [CrossRef]
    [Google Scholar]
  23. Makarova K. S., Aravind L., Wolf Y. I., Tatusov R. L., Minton K. W., Koonin E. V., Daly M. J. 2001; Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 65:44–79 [CrossRef]
    [Google Scholar]
  24. Markillie L. M., Varnum S. M., Hradecky P., Wong K. K. 1999; Targeted mutagenesis by duplication insertion in the radioresistant bacterium Deinococcus radiodurans : radiation sensitivities of catalase ( katA ) and superoxide dismutase ( sodA ) mutants. J Bacteriol 181:666–669
    [Google Scholar]
  25. Matsumura H., Takeyama H., Kusakabe E., Burgess J. G., Matsunaga T. 1997; Cloning, sequencing and expressing the carotenoid biosynthesis genes, lycopene cyclase and phytoene desaturase, from the aerobic photosynthetic bacterium Erythrobacter longus sp. strain Och101 in Escherichia coli. Gene 189:169–174 [CrossRef]
    [Google Scholar]
  26. Meima R., Lidstrom M. E. 2000; Characterization of the minimal replicon of a cryptic Deinococcus radiodurans SARK plasmid and development of versatile Escherichia coli - D. radiodurans shuttle vectors. Appl Environ Microbiol 66:3856–3867 [CrossRef]
    [Google Scholar]
  27. Melin A. M., Peuchant E., Perromat A., Clerc M. 1998; Sensitivity to oxidative damage of two Deinococcus radiodurans strains. J Appl Microbiol 84:531–537 [CrossRef]
    [Google Scholar]
  28. Meunier-Jamin C., Kapp U., Leonard G. A., McSweeney S. 2004; The structure of the organic hydroperoxide resistance protein from Deinococcus radiodurans . Do conformational changes facilitate recycling of the redox disulfide?. J Biol Chem 279:25830–25837 [CrossRef]
    [Google Scholar]
  29. Minton K. W. 1994; DNA repair in the extremely radioresistant bacterium Deinococcus radiodurans. Mol Microbiol 13:9–15 [CrossRef]
    [Google Scholar]
  30. Misawa N., Nakagawa M., Kobayashi K., Yamano S., Izawa Y., Nakamura K., Harashima K. 1990; Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172:6704–6712
    [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
    [Google Scholar]
  32. Misra H. S., Khairnar N. P., Barik A., Indira-Priyadarsini K., Mohan H., Apte S. K. 2004; Pyrroloquinoline-quinone: a reactive oxygen species scavenger in bacteria. FEBS Lett 578:26–30 [CrossRef]
    [Google Scholar]
  33. Mosely B. E. B. 1983; Photobiology and radiobiology of Micrococcus (Deinococcus) radiodurans. Photochem Photobiol Rev 7:223–275
    [Google Scholar]
  34. Narumi I., Satoh K., Cui S., Funayama T., Kitayama S., Watanabe H. 2004; PprA: a novel protein from Deinococcus radiodurans that stimulates DNA ligation. Mol Microbiol 54:278–285 [CrossRef]
    [Google Scholar]
  35. Palozza P. 1998; Prooxidant actions of carotenoids in biologic systems. Nutr Rev 56:257–265
    [Google Scholar]
  36. Ruiz-Hidalgo M. J., Benito E. P., Sandmann G., Eslava A. P. 1997; The phytoene dehydrogenase gene of Phycomyces : regulation of its expression by blue light and vitamin A. Mol Gen Genet 253:734–744 [CrossRef]
    [Google Scholar]
  37. Schneider C., Boger P., Sandmann G. 1997; Phytoene desaturase: heterologous expression in an active state, purification, and biochemical properties. Protein Expr Purif 10:175–179 [CrossRef]
    [Google Scholar]
  38. Stahl W., Junghans A., Driomina E. S., Briviba K., Sies H., de Boer B. 1998; Carotenoid mixtures protect multilamellar liposomes against oxidative damage: synergistic effects of lycopene and lutein. FEBS Lett 427:305–308 [CrossRef]
    [Google Scholar]
  39. Steiger S., Jackisch Y., Sandmann G. 2005; Carotenoid biosynthesis in Gloeobacter violaceus PCC4721 involves a single CrtI-type phytoene desaturase instead of typical cyanobacterial enzymes. Arch Microbiol 184:207–214 [CrossRef]
    [Google Scholar]
  40. Tao L., Cheng Q. 2004; Novel beta-carotene ketolases from non-photosynthetic bacteria for canthaxanthin synthesis. Mol Genet Genomics 272:530–537 [CrossRef]
    [Google Scholar]
  41. Tao L., Picataggio S., Rouviere P. E., Cheng Q. 2004; Asymmetrically acting lycopene beta-cyclases (CrtLm) from non-photosynthetic bacteria. Mol Genet Genomics 271:180–188 [CrossRef]
    [Google Scholar]
  42. Tian B., Wu Y., Sheng D., Zheng Z., Gao G., Hua Y. 2004; Chemiluminescence assay for reactive oxygen species scavenging activities and inhibition on oxidative damage of DNA in Deinococcus radiodurans. Luminescence 19:78–84 [CrossRef]
    [Google Scholar]
  43. Tsuchiya T., Takaichi S., Misawa N., Maoka T., Miyashita H., Mimuro M. 2005; The cyanobacterium Gloeobacter violaceus PCC 7421 uses bacterial-type phytoene desaturase in carotenoid biosynthesis. FEBS Lett 579:2125–2129 [CrossRef]
    [Google Scholar]
  44. White O., Eisen J. A., Heidelberg J. F., Hickey E. K., Peterson J. D., Dodson R. J., Haft D. H., Gwinn M. L., Nelson W. C. other authors 1999; Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577 [CrossRef]
    [Google Scholar]
  45. Yeh S., Hu M. 2000; Antioxidant and pro-oxidant effects of lycopene in comparison with beta-carotene on oxidant-induced damage in Hs68 cells. J Nutr Biochem 11:548–554 [CrossRef]
    [Google Scholar]
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