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Genetic control for light-induced carotenoid production in non-phototrophic bacteria

  • Original Paper - JMBM
  • Published:
Journal of Industrial Microbiology and Biotechnology

Abstract

Carotenoids are naturally occurring yellow or orange pigments that serve as a protectant against photo-oxidative damages. Among the wide variety of producers, the prokaryotes generate a broad spectrum of carotenoids with diverse chemical structures that are expected to have a high potential in biotechnological applications. Bacterial carotenogenesis occurs in a constitutive or light-induced manner, which suggests the diversity of the regulatory mechanism. The mechanism for light-induced carotenoid production in non-phototrophic bacteria has been studied in detail in Myxococcus xanthus, a Gram-negative gliding bacterium. The complicated mechanism involves the activation of an extracytoplasmic function (ECF) sigma factor (CarQ), which leads to the sequestration of a MerR family transcriptional regulator (CarA) that represses the expression of the carotenoid biosynthesis genes in the dark. Recently, we identified another regulatory mechanism for light-induced carotenogenesis in Streptomyces coelicolor A3(2), a Gram-positive soil bacterium. In this organism, the transcription of the carotenoid biosynthesis gene cluster is specified by LitS, a photo-inducible ECF sigma factor. The evidence indicates that the photo-dependent transcription of litS is mediated by LitR, a MerR family transcriptional regulator. In addition, it is suggested that the conformational alteration of LitR upon receiving the illumination signal determines its binding to DNA. The carboxy-terminal domain of LitR contains a possible binding site for Vitamin B12, which may serve as a capturing apparatus for the illumination signal.

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References

  1. 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 

  2. Armstrong GA (1994) Eubacteria show their true colors: genetics of carotenoid pigment biosynthesis from microbes to plants. J Bacteriol 176:4795–4802

    PubMed  CAS  Google Scholar 

  3. Armstrong GA (1997) Genetics of eubacterial carotenoid biosynthesis: a colorful tale. Annu Rev Microbiol 51:629–659

    Article  PubMed  CAS  Google Scholar 

  4. Asker D, Ohta Y (2002) Haloferax alexandrinus sp nov, an extremely halophilic canthaxanthin-producing archaeon from a solar saltern in Alexandria (Egypt). Int J Syst Evol Microbiol 52:729–738

    Article  PubMed  CAS  Google Scholar 

  5. Asker D, Ohta Y (2002) Production of canthaxanthin by Haloferax alexandrinus under non-aseptic conditions and a simple, rapid method for its extraction. Appl Microbiol Biotechnol 58:743–750

    Article  PubMed  CAS  Google Scholar 

  6. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  PubMed  Google Scholar 

  7. Berry A, Janssens D, Humbelin M, Jore JPM, Hoste B, Cleenwerck I, Vancanneyt M, Bretzel W, Mayer AF, Lopez-Ulibarri R, Shanmugam B, Swings J, Pasamontes L (2003) Paracoccus zeaxanthinifaciens sp. nov., a zeaxanthin-producing bacterium. Int J Syst Evol Microbiol 53:231–238

    Article  PubMed  CAS  Google Scholar 

  8. Brown NL, Stoyanov JV, Kidd SP, Hobman JL (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27:145–163

    Article  PubMed  CAS  Google Scholar 

  9. Browning DF, Whitworth DE, Hodgson DA (2003) Light-induced carotenogenesis in Myxococcus xanthus: functional characterization of the ECF sigma factor CarQ and antisigma factor CarR. Mol Microbiol 48:237–251

    Article  PubMed  CAS  Google Scholar 

  10. Burchard RP, Dworkin M (1966) Light-induced lysis and carotenogenesis in Myxococcus xanthus. J Bacteriol 91:535–545

    PubMed  CAS  Google Scholar 

  11. Calo P, de Miguel T, Sieiro CB, Velázquez JB, Villa TG (1995) Ketocarotenoids in halobacteria: 3-hydroxy echinenone and trans-astaxanthin. J Appl Bacteriol 79:282–285

    CAS  Google Scholar 

  12. Cervantes M, Murillo FJ (2002) Role for vitamin B(12) in light induction of gene expression in the bacterium Myxococcus xanthus. J Bacteriol 184:2215–2224

    Article  PubMed  CAS  Google Scholar 

  13. Chater KF (1993) Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47:685–713

    Article  PubMed  CAS  Google Scholar 

  14. Cooney JJ, Marks JHW, Smith AM (1966) Isolation and identification of canthaxanthin from Micrococcus roseus. J Bacteriol 92:342–345

    CAS  Google Scholar 

  15. Fontes M, Galbis-Martinez L, Murillo FJ (2003) A novel regulatory gene for light-induced carotenoid synthesis in the bacterium Myxococcus xanthus. Mol Microbiol 47:561–571

    Article  PubMed  CAS  Google Scholar 

  16. Galbis-Martinez M, Fontes M, Murillo FJ (2004) The high-mobility group A-type protein carD of the bacterium Myxococcus xanthus as a transcription factor for several distinct vegetative genes. Genetics 167:1585–1595

    Article  PubMed  CAS  Google Scholar 

  17. Goodwin TW (1980) Non-photosynthetic bacteria. In: Goodwin TW (ed) The biochemistry of the carotenoids. Chapman & Hall Ltd, London, pp 290–317

    Google Scholar 

  18. Gorham HC, McGowan SJ, Robson PR, Hodgson DA (1996) Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol Microbiol 19:171–186

    Article  PubMed  CAS  Google Scholar 

  19. Grogan DW (1989) Phenotypic characterization of the archaebacterial genus Sulfolobus: comparison of five wild-type strains. J Bacteriol 171:6710–6719

    PubMed  CAS  Google Scholar 

  20. Harker M, Hirschberg J, Oren A (1998) Paracoccus marcusii sp. nov., an orange gram-negative coccus. Int J Syst Bacteriol 48:543–548

    PubMed  Google Scholar 

  21. 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 

  22. Hodgson DA, Murillo FJ (1993) Genetics of regulation and pathway of synthesis of carotenoids. In: Dworkin M, Kaiser D (eds) Myxobacteria II. American Society for Microbiology, Washington, pp 157–181

    Google Scholar 

  23. Hundle BS, O’Brien DA, Beyer P, Kleinig H, Hearst JE (1993) In vitro expression and activity of lycopene cyclase and beta-carotene hydroxylase from Erwinia herbicola. FEBS Lett 315:329–334

    Article  PubMed  CAS  Google Scholar 

  24. Iizuka H, Nishimura Y (1969) Microbiological studies on petroleum and natural gas X Carotenoid pigments of hydrocarbon utilizing bacteria. J Gen Appl Microbiol 15:127–134

    CAS  Google Scholar 

  25. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Ōmura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531

    Article  PubMed  Google Scholar 

  26. Jarret JT, Goulding CW, Fluhr K, Huang S, Mathews RG (1997) Purification and assay of cobalamin-dependent methionine synthase from Escherichia coli. Methods Enzymol 281:196–213

    Article  PubMed  Google Scholar 

  27. Kaiser D, Manoil C, Dworkin M (1979) Myxobacteria: cell interactions, genetics, and development. Annu Rev Microbiol 33:595–639

    Article  PubMed  CAS  Google Scholar 

  28. Kato F, Hino T, Nakaji A, Tanaka M, Koyama Y (1995) Carotenoid synthesis in Streptomyces setonii ISP5395 is induced by the gene crtS, whose product is similar to a sigma factor. Mol Gen Genet 247:387–390

    Article  PubMed  CAS  Google Scholar 

  29. Koyama Y, Kato F, Yazawa Y (1976) Effect of light on the pigmentation of bacteria in Actinomycetales. Toppan, Tokyo

    Google Scholar 

  30. Krubasik P, Takaichi S, Maoka T, Kobayashi M, Masamoto K, Sandmann G (2001) Detailed biosynthetic pathway to decaprenoxanthin diglucoside in Corynebacterium glutamicum and identification of novel intermediates. Arch Microbiol 176:217–223

    Article  PubMed  CAS  Google Scholar 

  31. 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 

  32. Kull DR, Pfander H (1997) Isolation and structure elucidation of carotenoid glycosides from the thermoacidophilic archaea Sulfolobus shibatae. J Nat Prod 60:371–374

    Article  CAS  Google Scholar 

  33. Lagarde D, Beuf L, Vermaas W (2000) Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 66:64–72

    PubMed  CAS  Google Scholar 

  34. Lee HS, Ohnishi Y, Horinouchi S (2001) A σB-like factor responsible for carotenoid biosynthesis in Streptomyces griseus. J Mol Microbiol Biotechnol 3:95–101

    PubMed  CAS  Google Scholar 

  35. Lee JH, Kim YS, Choi TJ, Lee WJ, Kim YT (2004) Paracoccus haeundaensis sp. nov., a Gram-negative, halophilic, astaxanthin-producing bacterium. Int J Syst Evol Microbiol 54:1699–1702

    Article  PubMed  CAS  Google Scholar 

  36. Lorquin J, Molouba F, Dreyfus BL (1997) Identification of the carotenoid pigment canthaxanthin from photosynthetic Bradyrhizobium strains. App Environ Microbiol 63: 1151–1154

    CAS  Google Scholar 

  37. McDermott JC, Britton G, Goodwin TW (1973) Carotenoid biosynthesis in a Flavobacterium sp: stereochemistry of hydrogen elimination in the desaturation of phytoene to lycopene, rubixanthin and zeaxanthin. Biochem J 134:1115–1117

    PubMed  CAS  Google Scholar 

  38. Miyadoh S (1993) Research on antibiotic screening in Japan over the last decade: a producing microorganisms approach. Actinomycetologica 7:100–106

    Google Scholar 

  39. Moreno AJ, Fontes M, Murillo FJ (2001) ihfA gene of the bacterium Myxococcus xanthus and its role in activation of carotenoid genes by blue light. J Bacteriol 183:557–569

    Article  PubMed  CAS  Google Scholar 

  40. Nelis HJ, De Leenheer AP (1989) Reinvestigation of Brevibacterium sp. strain KY-4313 as a source of canthaxanthin. Appl Environ Microbiol 55:2505–2510

    PubMed  CAS  Google Scholar 

  41. Rilling HC (1962) Photoinduction of carotenoid synthesis of a Mycobacterium sp. Biochim Biophys Acta 60:548–556

    Article  PubMed  CAS  Google Scholar 

  42. Ronnekleiv M (1995) Bacterial carotenoids 53 C50-carotenoids 23; carotenoids of Haloferax volcanii versus other halophilic bacteria. Biochem Syst Ecol 23:627–634

    Article  CAS  Google Scholar 

  43. Sakurai H, Kato K, Sakai T, Masuda Y, Kuriyama T (1971) Studies on microbial utilization of petroleum I separation and characterization of carotenoids produced by a species of Brevibacterium in hydrocarbon media. Bull Chem Soc Japan 44:481–484

    Article  CAS  Google Scholar 

  44. Schmidt K (1978) Biosynthesis of carotenoids. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum, New York, pp 729–750

    Google Scholar 

  45. Schmidt K (1980) A comparative study on the composition of chlorosomes (chlorobium vesicles) and cytoplasmic membranes from Chloroflexus aurantiacus strain Ok-70-f1 and Chlorobium limicola f. thiosulfatophilum strain 6230. Arch Microbiol 124:21–31

    Article  CAS  Google Scholar 

  46. Schumann G, Nurnberger H, Sandmann G, Krugel H (1996) Activation and analysis of cryptic crt genes for carotenoid biosynthesis from Streptomyces griseus. Mol Gen Genet 252:658–666

    PubMed  CAS  Google Scholar 

  47. Strand A, Shivaji S, Liaaen-Jensen S (1997) Bacterial carotenoids 55. C50-carotenoids 25. revised structures of carotenoids associated with membranes in psychrotrophic Micrococcus roseus. Biochem Syst Ecol 25:547–552

    Article  CAS  Google Scholar 

  48. Takaichi S, Shimada K, Ishidsu J (1990) Carotenoids from the aerobic photosynthetic bacterium, Erythrobacter longus: beta-caroptene and its hydroxy derivatives. Arch Microbiol 153:118–122

    Article  CAS  Google Scholar 

  49. Takano H, Obitsu S, Beppu T, Ueda K (2005) Light-induced carotenogenesis in Streptomyces coelicolor A3(2): identification of an extracytoplasmic function sigma factor that directs photodependent transcription of the carotenoid biosynthesis gene cluster. J Bacteriol 187:1825–1832

    Article  PubMed  CAS  Google Scholar 

  50. Tsubokura A, Yoneda H, Mizuta H (1999) Paracoccus carotinifaciens sp nov, a new aerobic gram-negative astaxanthin-producing bacterium. Int J Syst Bacteriol 49:277–282

    Article  PubMed  CAS  Google Scholar 

  51. Weeks OB, Garner RJ (1967) Biosynthesis of carotenoids in Flavobacterium dehydrogenans Arnaudi. Arch Biochem Biophys 121:35–49

    Article  PubMed  CAS  Google Scholar 

  52. Whitworth DE, Hodgson DA (2001) Light-induced carotenogenesis in Myxococcus xanthus: evidence that CarS acts as an anti-repressor of CarA. Mol Microbiol 42:809–819

    Article  PubMed  CAS  Google Scholar 

  53. Yokoyama A, Izumida H, Miki W (1994) Production of astaxanthin and 4-ketozeaxanthin by the marine bacterium, Agrobacterium aurantiacum. Biosci Biotech Biochem 58:1842–1844

    Article  CAS  Google Scholar 

  54. 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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Acknowledgements

We thank D. A. Hodgson for providing helpful information. This study was supported by the 21st century COE program of MEXT, Japan. D. A. was supported by a JSPS grant.

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Correspondence to Kenji Ueda.

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Takano, H., Asker, D., Beppu, T. et al. Genetic control for light-induced carotenoid production in non-phototrophic bacteria. J IND MICROBIOL BIOTECHNOL 33, 88–93 (2006). https://doi.org/10.1007/s10295-005-0005-z

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  • DOI: https://doi.org/10.1007/s10295-005-0005-z

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