Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1993 Apr;12(4):1265–1275. doi: 10.1002/j.1460-2075.1993.tb05771.x

Growth phase dependence of the activation of a bacterial gene for carotenoid synthesis by blue light.

M Fontes 1, R Ruiz-Vázquez 1, F J Murillo 1
PMCID: PMC413336  PMID: 8467787

Abstract

Myxococcus xanthus responds to blue light by producing carotenoid pigments. A mutation at a gene named carC is known to block the metabolism of phytoene, a carotenoid precursor, and this gene has now been cloned and sequenced. We show here that gene carC, which is homologous to phytoene dehydrogenase genes from other organisms, is tightly regulated by light through a mechanism that operates only when the cells have reached the stationary phase or are starved of a carbon source. A genetic element that mediates the effect of the growth phase has been identified. Gene carC is integrated with another unlinked carotenogenic gene in a single 'light regulon' controlled by common trans-acting genetic elements. A potential -35 site for the binding of sigma factors has been found upstream of the carC transcriptional start. However, the -10 region shows no similarity with analogous sites at promoters of other Gram-negative bacteria.

Full text

PDF
1265

Images in this article

1268Image
on p.1268

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aldea M., Garrido T., Pla J., Vicente M. Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters. EMBO J. 1990 Nov;9(11):3787–3794. doi: 10.1002/j.1460-2075.1990.tb07592.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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 U S A. 1990 Dec;87(24):9975–9979. doi: 10.1073/pnas.87.24.9975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong G. A., Alberti M., Leach F., Hearst J. E. Nucleotide sequence, organization, and nature of the protein products of the carotenoid biosynthesis gene cluster of Rhodobacter capsulatus. Mol Gen Genet. 1989 Apr;216(2-3):254–268. doi: 10.1007/BF00334364. [DOI] [PubMed] [Google Scholar]
  4. Avery L., Kaiser D. In situ transposon replacement and isolation of a spontaneous tandem genetic duplication. Mol Gen Genet. 1983;191(1):99–109. doi: 10.1007/BF00330896. [DOI] [PubMed] [Google Scholar]
  5. Balsalobre J. M., Ruiz-Vazquez R. M., Murillo F. J. Light induction of gene expression in Myxococcus xanthus. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2359–2362. doi: 10.1073/pnas.84.8.2359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bibb M. J., Findlay P. R., Johnson M. W. The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene. 1984 Oct;30(1-3):157–166. doi: 10.1016/0378-1119(84)90116-1. [DOI] [PubMed] [Google Scholar]
  7. Biel A. J., Marrs B. L. Oxygen does not directly regulate carotenoid biosynthesis in Rhodopseudomonas capsulata. J Bacteriol. 1985 Jun;162(3):1320–1321. doi: 10.1128/jb.162.3.1320-1321.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bohannon D. E., Connell N., Keener J., Tormo A., Espinosa-Urgel M., Zambrano M. M., Kolter R. Stationary-phase-inducible "gearbox" promoters: differential effects of katF mutations and role of sigma 70. J Bacteriol. 1991 Jul;173(14):4482–4492. doi: 10.1128/jb.173.14.4482-4492.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bramley P. M., Mackenzie A. Regulation of carotenoid biosynthesis. Curr Top Cell Regul. 1988;29:291–343. doi: 10.1016/b978-0-12-152829-4.50009-4. [DOI] [PubMed] [Google Scholar]
  10. Bretscher A. P., Kaiser D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J Bacteriol. 1978 Feb;133(2):763–768. doi: 10.1128/jb.133.2.763-768.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Burchard R. P., Dworkin M. Light-induced lysis and carotenogenesis in Myxococcus xanthus. J Bacteriol. 1966 Feb;91(2):535–545. doi: 10.1128/jb.91.2.535-545.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Burchard R. P., Hendricks S. B. Action spectrum for carotenogenesis in Myxococcus xanthus. J Bacteriol. 1969 Mar;97(3):1165–1168. doi: 10.1128/jb.97.3.1165-1168.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  14. Demple B. Regulation of bacterial oxidative stress genes. Annu Rev Genet. 1991;25:315–337. doi: 10.1146/annurev.ge.25.120191.001531. [DOI] [PubMed] [Google Scholar]
  15. Di Mascio P., Kaiser S., Sies H. Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys. 1989 Nov 1;274(2):532–538. doi: 10.1016/0003-9861(89)90467-0. [DOI] [PubMed] [Google Scholar]
  16. Erickson J. W., Gross C. A. Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev. 1989 Sep;3(9):1462–1471. doi: 10.1101/gad.3.9.1462. [DOI] [PubMed] [Google Scholar]
  17. Farr S. B., Kogoma T. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev. 1991 Dec;55(4):561–585. doi: 10.1128/mr.55.4.561-585.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gill R. E., Cull M. G., Fly S. Genetic identification and cloning of a gene required for developmental cell interactions in Myxococcus xanthus. J Bacteriol. 1988 Nov;170(11):5279–5288. doi: 10.1128/jb.170.11.5279-5288.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem. 1988;57:199–233. doi: 10.1146/annurev.bi.57.070188.001215. [DOI] [PubMed] [Google Scholar]
  20. Helmann J. D., Chamberlin M. J. Structure and function of bacterial sigma factors. Annu Rev Biochem. 1988;57:839–872. doi: 10.1146/annurev.bi.57.070188.004203. [DOI] [PubMed] [Google Scholar]
  21. Inouye S. Identification of a development-specific promoter of Myxococcus xanthus. J Mol Biol. 1984 Mar 25;174(1):113–120. doi: 10.1016/0022-2836(84)90367-x. [DOI] [PubMed] [Google Scholar]
  22. Komano T., Franceschini T., Inouye S. Identification of a vegetative promoter in Myxococcus xanthus. A protein that has homology to histones. J Mol Biol. 1987 Aug 5;196(3):517–524. doi: 10.1016/0022-2836(87)90029-5. [DOI] [PubMed] [Google Scholar]
  23. Kroos L., Kaiser D. Construction of Tn5 lac, a transposon that fuses lacZ expression to exogenous promoters, and its introduction into Myxococcus xanthus. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5816–5820. doi: 10.1073/pnas.81.18.5816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kuspa A., Kroos L., Kaiser D. Intercellular signaling is required for developmental gene expression in Myxococcus xanthus. Dev Biol. 1986 Sep;117(1):267–276. doi: 10.1016/0012-1606(86)90369-6. [DOI] [PubMed] [Google Scholar]
  25. Lange R., Hengge-Aronis R. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol. 1991 Jul;173(14):4474–4481. doi: 10.1128/jb.173.14.4474-4481.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Martinez-Laborda A., Murillo F. J. Genic and allelic interactions in the carotenogenic response of myxococcus xanthus to blue light. Genetics. 1989 Jul;122(3):481–490. doi: 10.1093/genetics/122.3.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Martínez-Laborda A., Balsalobre J. M., Fontes M., Murillo F. J. Accumulation of carotenoids in structural and regulatory mutants of the bacterium Myxococcus xanthus. Mol Gen Genet. 1990 Sep;223(2):205–210. doi: 10.1007/BF00265055. [DOI] [PubMed] [Google Scholar]
  28. 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 Dec;172(12):6704–6712. doi: 10.1128/jb.172.12.6704-6712.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Morett E., Buck M. In vivo studies on the interaction of RNA polymerase-sigma 54 with the Klebsiella pneumoniae and Rhizobium meliloti nifH promoters. The role of NifA in the formation of an open promoter complex. J Mol Biol. 1989 Nov 5;210(1):65–77. doi: 10.1016/0022-2836(89)90291-x. [DOI] [PubMed] [Google Scholar]
  30. Mulvey M. R., Loewen P. C. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor. Nucleic Acids Res. 1989 Dec 11;17(23):9979–9991. doi: 10.1093/nar/17.23.9979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nelson M. A., Morelli G., Carattoli A., Romano N., Macino G. Molecular cloning of a Neurospora crassa carotenoid biosynthetic gene (albino-3) regulated by blue light and the products of the white collar genes. Mol Cell Biol. 1989 Mar;9(3):1271–1276. doi: 10.1128/mcb.9.3.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Reznikoff W. S., Siegele D. A., Cowing D. W., Gross C. A. The regulation of transcription initiation in bacteria. Annu Rev Genet. 1985;19:355–387. doi: 10.1146/annurev.ge.19.120185.002035. [DOI] [PubMed] [Google Scholar]
  33. Romeo J. M., Zusman D. R. Transcription of the myxobacterial hemagglutinin gene is mediated by a sigma 54-like promoter and a cis-acting upstream regulatory region of DNA. J Bacteriol. 1991 May;173(9):2969–2976. doi: 10.1128/jb.173.9.2969-2976.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rosner J. L. Formation, induction, and curing of bacteriophage P1 lysogens. Virology. 1972 Jun;48(3):679–689. doi: 10.1016/0042-6822(72)90152-3. [DOI] [PubMed] [Google Scholar]
  35. Ruiz-Vázquez R., Murillo F. J. Abnormal motility and fruiting behavior of Myxococcus xanthus bacteriophage-resistant strains induced by a clear-plaque mutant of bacteriophage Mx8. J Bacteriol. 1984 Nov;160(2):818–821. doi: 10.1128/jb.160.2.818-821.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schmidhauser T. J., Lauter F. R., Russo V. E., Yanofsky C. Cloning, sequence, and photoregulation of al-1, a carotenoid biosynthetic gene of Neurospora crassa. Mol Cell Biol. 1990 Oct;10(10):5064–5070. doi: 10.1128/mcb.10.10.5064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shimkets L. J., Gill R. E., Kaiser D. Developmental cell interactions in Myxococcus xanthus and the spoC locus. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1406–1410. doi: 10.1073/pnas.80.5.1406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stephens K., Hartzell P., Kaiser D. Gliding motility in Myxococcus xanthus: mgl locus, RNA, and predicted protein products. J Bacteriol. 1989 Feb;171(2):819–830. doi: 10.1128/jb.171.2.819-830.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Vicente M., Kushner S. R., Garrido T., Aldea M. The role of the 'gearbox' in the transcription of essential genes. Mol Microbiol. 1991 Sep;5(9):2085–2091. doi: 10.1111/j.1365-2958.1991.tb02137.x. [DOI] [PubMed] [Google Scholar]
  41. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  42. Yanofsky C., Platt T., Crawford I. P., Nichols B. P., Christie G. E., Horowitz H., VanCleemput M., Wu A. M. The complete nucleotide sequence of the tryptophan operon of Escherichia coli. Nucleic Acids Res. 1981 Dec 21;9(24):6647–6668. doi: 10.1093/nar/9.24.6647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yee T., Inouye M. Reexamination of the genome size of myxobacteria, including the use of a new method for genome size analysis. J Bacteriol. 1981 Mar;145(3):1257–1265. doi: 10.1128/jb.145.3.1257-1265.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES