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CYP287A1 is a carotenoid 2-β-hydroxylase required for deinoxanthin biosynthesis in Deinococcus radiodurans R1

  • Applied genetics and molecular biotechnology
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Abstract

The carotenoid deinoxanthin is a crucial resistance factor against various stresses in the radiation-resistant bacterium Deinococcus radiodurans. Disruption of the gene dr2473 encoding the cytochrome P450 CYP287A1 led to the accumulation of 2-deoxydeinoxanthin in D. radiodurans, demonstrating that CYP287A1 is a novel β-carotene 2-hydroxylase. The dr2473 knockout mutant was shown to be more sensitive to UV radiation and oxidative stress than the wild-type strain D. radiodurans R1, indicating that the C2 alcohol of deinoxanthin is important for antioxidant activity.

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References

  • Aasen AJ, Jensen SL (1966) Carotenoids of flexibacteria. 3. The structures of flexixanthin and deoxy-flexixanthin. Acta Chem Scand 20:1970–1988

    Article  CAS  PubMed  Google Scholar 

  • Albrecht M, Takaichi S, Steiger S, Wang ZY, Sandmann G (2000) Novel hydroxycarotenoids with improved antioxidative properties produced by gene combination in Escherichia coli. Nat Biotechnol 18:843–846. doi:10.1038/78443

    Article  CAS  PubMed  Google Scholar 

  • Alvarez V, Rodriguez-Saiz M, de la Fuente JL, Gudina EJ, Godio RP, Martin JF, Barredo JL (2006) The crtS gene of Xanthophyllomyces dendrorhous encodes a novel cytochrome-P450 hydroxylase involved in the conversion of beta-carotene into astaxanthin and other xanthophylls. Fungal Genet Biol 43:261–272. doi:10.1016/j.fgb.2005.12.004

    Article  CAS  PubMed  Google Scholar 

  • Blasco F, Kauffmann I, Schmid RD (2004) CYP175A1 from Thermus thermophilus HB27, the first beta-carotene hydroxylase of the P450 superfamily. Appl Microbiol Biotechnol 64:671–674. doi:10.1007/s00253-003-1529-7

    Article  CAS  PubMed  Google Scholar 

  • Cox MM, Battista JR (2005) Deinococcus radiodurans—the consummate survivor. Nat Rev Microbiol 3:882–892. doi:10.1038/nrmicro1264

    Article  CAS  PubMed  Google Scholar 

  • Csernetics A, Toth E, Farkas A, Nagy G, Bencsik O, Vagvolgyi C, Papp T (2015) Expression of Xanthophyllomyces dendrorhous cytochrome-P450 hydroxylase and reductase in Mucor circinelloides. World J Microbiol Biotechnol 31:321–336. doi:10.1007/s11274-014-1784-z

    Article  CAS  PubMed  Google Scholar 

  • Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583. doi:10.1146/annurev.arplant.49.1.557

    Article  CAS  PubMed  Google Scholar 

  • Davison PA, Hunter CN, Horton P (2002) Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206. doi:10.1038/nature00861

    Article  CAS  PubMed  Google Scholar 

  • Fairand BP, Fidopiastis N (2010) Radiation sterilization of aseptically manufactured products. PDA J Pharm Sci Technol 64:299–304

    CAS  PubMed  Google Scholar 

  • 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 doi:S0921877799000440

  • Ghosal D, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Venkateswaran A, Zhai M, Kostandarithes HM, Brim H, Makarova KS, Wackett LP, Fredrickson JK, Daly MJ (2005) How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol Rev 29:361–375. doi:10.1016/j.femsre.2004.12.007

    CAS  PubMed  Google Scholar 

  • Gotz T, Sandmann G, Romer S (2002) Expression of a bacterial carotene hydroxylase gene (crtZ) enhances UV tolerance in tobacco. Plant Mol Biol 50:129–142

    Article  PubMed  Google Scholar 

  • Jovanovic Z, Jovanovic S (2013) A comparison of the effects of cumene hydroperoxide and hydrogen peroxide on Retzius nerve cells of the leech Haemopis sanguisuga. Exp Anim 62:9–17 doi:DN/JST.JSTAGE/expanim/62.9

  • Lee GY, Kim DH, Kim D, Ahn T, Yun CH (2015) Functional characterization of steroid hydroxylase CYP106A1 derived from Bacillus megaterium. Arch Pharm Res 38:98–107. doi:10.1007/s12272-014-0366-9

    Article  CAS  PubMed  Google Scholar 

  • Lemee L, Peuchant E, Clerc M, Brunner M, Pfander H (1997) Deinoxanthin: a new carotenoid isolated from Deinococcus radiodurans. Tetrahedron 53:919–926

    Article  CAS  Google Scholar 

  • Miki Y, Asano Y (2014) Biosynthetic pathway for the cyanide-free production of phenylacetonitrile in Escherichia coli by utilizing plant cytochrome P450 79A2 and bacterial aldoxime dehydratase. Appl Environ Microbiol 80:6828–6836. doi:10.1128/AEM.01623-14

    Article  PubMed Central  PubMed  Google Scholar 

  • Molnár I, Hill DS, Zirkle R, Hammer PE, Gross F, Buckel TG, Jungmann V, Pachlatko JP, Ligon JM (2005) Biocatalytic conversion of avermectin to 4″-oxo-avermectin: heterologous expression of the ema1 cytochrome P450 monooxygenase. Appl Environ Microbiol 71:6977–6985

    Article  PubMed Central  PubMed  Google Scholar 

  • Narumi I, Satoh K, Kikuchi M, Funayama T, Kitayama S, Yanagisawa T, Watanabe H, Yamamoto K (1999) Molecular analysis of the Deinococcus radiodurans recA locus and identification of a mutation site in a DNA repair-deficient mutant, rec30. Mutat Res 435:233–243 doi:S0921877799000488

  • Nelson DR (2011) Progress in tracing the evolutionary paths of cytochrome P450. Biochim Biophys Acta 1814(1):14–18

  • 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 71:4286–4296. doi:10.1128/AEM.71.8.4286-4296.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pan J, Wang J, Zhou Z, Yan Y, Zhang W, Lu W, Ping S, Dai Q, Yuan M, Feng B, Hou X, Zhang Y, Ma R, Liu T, Feng L, Wang L, Chen M, Lin M (2009) IrrE, a global regulator of extreme radiation resistance in Deinococcus radiodurans, enhances salt tolerance in Escherichia coli and Brassica napus. PLoS One 4:e4422 doi:10.1371/journal.pone.0004422

  • Saito T, Ohyama Y, Ide H, Ohta S, Yamamoto O (1998) A carotenoid pigment of the radioresistant bacterium Deinococcus radiodurans. Microbios 95:79–90

    CAS  Google Scholar 

  • Schoefs B, Rmiki N, Rachadi J, Lemoine Y (2001) Astaxanthin accumulation in Haematococcus requires a cytochrome P450 hydroxylase and an active synthesis of fatty acids. FEBS Lett 500:125–128 doi:S0014579301025960

  • Slade D, Lindner AB, Paul G, Radman M (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136:1044–1055. doi:10.1016/j.cell.2009.01.018

    Article  CAS  PubMed  Google Scholar 

  • Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191. doi:10.1128/MMBR.00015-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takaichi S, Mochimaru M (2007) Carotenoids and carotenogenesis in cyanobacteria: unique ketocarotenoids and carotenoid glycosides. Cell Mol Life Sci 64:2607–2619. doi:10.1007/s00018-007-7190-z

    Article  CAS  PubMed  Google Scholar 

  • Tian B, Hua Y (2010) Carotenoid biosynthesis in extremophilic Deinococcus-Thermus bacteria. Trends Microbiol 18:512–520. doi:10.1016/j.tim.2010.07.007

    Article  CAS  PubMed  Google Scholar 

  • Tian B, Sun Z, Xu Z, Shen S, Wang H, Hua Y (2008) Carotenoid 3′- 4′-desaturase is involved in carotenoid biosynthesis in the radioresistant bacterium Deinococcus radiodurans. Microbiology 154:3697–3706

    Article  CAS  PubMed  Google Scholar 

  • Tian B, Xu Z, Sun Z, Lin J, Hua Y (2007) Evaluation of the antioxidant effects of carotenoids from Deinococcus radiodurans through targeted mutagenesis, chemiluminescence, and DNA damage analyses. Biochim Biophys Acta 1770:902–911. doi:10.1016/j.bbagen.2007.01.016

    Article  CAS  PubMed  Google Scholar 

  • Tian L, DellaPenna D (2004) Progress in understanding the origin and functions of carotenoid hydroxylases in plants. Arch Biochem Biophys 430:22–29. doi:10.1016/j.abb.2004.02.003

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Xu Y, Maine EA, Wijeratne EM, Espinosa-Artiles P, Gunatilaka AA, Molnár I (2008) Functional characterization of the biosynthesis of radicicol, an Hsp90 inhibitor resorcylic acid lactone from Chaetomium chiversii. Chem Biol 15:1328–1338. doi:10.1016/j.chembiol.2008.10.006

    Article  CAS  PubMed  Google Scholar 

  • Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol. 2000;1(6):REVIEWS3003. Epub 2000 Dec 8 doi:10.1186/gb-2000–1–6-reviews3003

  • White O, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD, Dodson RJ, Haft DH, Gwinn ML, Nelson WC, Richardson DL, Moffat KS, Qin H, Jiang L, Pamphile W, Crosby M, Shen M, Vamathevan JJ, Lam P, McDonald L, Utterback T, Zalewski C, Makarova KS, Aravind L, Daly MJ, Minton KW, Fleischmann RD, Ketchum KA, Nelson KE, Salzberg S, Smith HO, Venter JC, Fraser CM (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577 doi:8014

  • Xu Y, Orozco R, Wijeratne EM, Gunatilaka AA, Stock SP, Molnár I (2008) Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus Beauveria bassiana. Chem Biol 15:898–907. doi:10.1016/j.chembiol.2008.07.011

    Article  CAS  PubMed  Google Scholar 

  • Zhu D, Tan KS, Zhang X, Sun AY, Sun GY, Lee JCM (2005) Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci 118:3695–3703

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Basic Research (973) Program of China (2015CB755700), the National High-Tech (863) Program of China (No. 2012AA02A703), the National Research and Development Project of Transgenic Crops of China (2014ZX08009-003), the National Natural Science Foundation of China (No. 31170105), and the US National Science Foundation (MCB-0948751 to IM).

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Funding

This work was supported by grants from the National Basic Research (973) Program of China (2015CB755700), and the National High-Tech (863) Program of China (No. 2012AA02A703), and the National Research and Development Project of Transgenic Crops of China (2014ZX08009-003), the National Natural Science Foundation of China (No. 31170105), and the US National Science Foundation (MCB-0948751 to IM).

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The authors declare that they have no competing interests.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Correspondence to István Molnár or Yuquan Xu.

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Zhengfu Zhou and Wei Zhang contributed equally to this work.

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Zhou, Z., Zhang, W., Su, S. et al. CYP287A1 is a carotenoid 2-β-hydroxylase required for deinoxanthin biosynthesis in Deinococcus radiodurans R1. Appl Microbiol Biotechnol 99, 10539–10546 (2015). https://doi.org/10.1007/s00253-015-6910-9

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