Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1985 Oct;164(1):45–50. doi: 10.1128/jb.164.1.45-50.1985

Control of Vibrio fischeri luminescence gene expression in Escherichia coli by cyclic AMP and cyclic AMP receptor protein.

P V Dunlap, E P Greenberg
PMCID: PMC214208  PMID: 2995319

Abstract

Under certain conditions glucose represses the autoinducible synthesis of luminescence enzymes in Vibrio fischeri. To examine the genetic regulation of luminescence more closely, Escherichia coli catabolite repression mutants were transformed with a plasmid (pJE202) that contains V. fischeri genes specifying the luminescence enzymes and encoding regulatory functions for luminescence (the lux genes) or with plasmids (pJE413 and pJE455) containing transcriptional fusions between the lacZ gene on transposon mini-Mu and specific genes in each of the two lux operons. Unless cyclic AMP (cAMP) was added to the growth medium, an adenylate cyclase deletion mutant containing pJE202 produced very little light and low levels of the light-emitting enzyme luciferase. When grown in the presence or absence of cAMP, a cAMP receptor protein (CRP) deletion mutant produced low levels of light and luciferase. A mutant that does not make cAMP but does make an altered CRP which does not require cAMP for activity produced induced levels of luminescence after transformation with pJE202. To test the effects of cAMP and CRP on each of the two lux operons separately rather than on both together, the E. coli catabolite repression mutants were transformed with pJE413 and pJE455. From measurements of beta-galactosidase and luciferase activities it appeared that cAMP and CRP affected transcription of both lux operons. In the presence of autoinducer and its receptor, transcription of the operon encoding all of the luminescence genes except the receptor gene appeared to be activated by cAMP and CRP, whereas in the absence of the receptor, cAMP and CRP appeared to decrease transcription of this operon. Transcription of the operon encoding the autoinducer receptor appeared to be stimulated by cAMP and CRP in the absence of the receptor itself. These results demonstrate that cAMP and CRP are required for proper control of the V. fischeri luminescence system and suggest that lux gene transcription is required by a complex mechanism.

Full text

PDF
46

Selected References

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

  1. Anderson W. B., Pastan I. The cyclic AMP receptor of Escherichia coli: immunological studies in extracts of Escherichia coli and other organisms. Biochim Biophys Acta. 1973 Oct 5;320(3):577–587. doi: 10.1016/0304-4165(73)90137-2. [DOI] [PubMed] [Google Scholar]
  2. Brickman E., Soll L., Beckwith J. Genetic characterization of mutations which affect catabolite-sensitive operons in Escherichia coli, including deletions of the gene for adenyl cyclase. J Bacteriol. 1973 Nov;116(2):582–587. doi: 10.1128/jb.116.2.582-587.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Casadaban M. J. Fusion of the Escherichia coli lac genes to the ara promoter: a general technique using bacteriophage Mu-1 insertions. Proc Natl Acad Sci U S A. 1975 Mar;72(3):809–813. doi: 10.1073/pnas.72.3.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dunlap P. V. Osmotic control of luminescence and growth in Photobacterium leiognathi from ponyfish light organs. Arch Microbiol. 1985 Feb;141(1):44–50. doi: 10.1007/BF00446738. [DOI] [PubMed] [Google Scholar]
  6. Eberhard A., Burlingame A. L., Eberhard C., Kenyon G. L., Nealson K. H., Oppenheimer N. J. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry. 1981 Apr 28;20(9):2444–2449. doi: 10.1021/bi00512a013. [DOI] [PubMed] [Google Scholar]
  7. Engebrecht J., Nealson K., Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell. 1983 Mar;32(3):773–781. doi: 10.1016/0092-8674(83)90063-6. [DOI] [PubMed] [Google Scholar]
  8. Engebrecht J., Silverman M. Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4154–4158. doi: 10.1073/pnas.81.13.4154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Henry J. P., Michelson A. M. Etudes de bioluminescence. Régulation de la bioluminescence bactérienne. C R Acad Sci Hebd Seances Acad Sci D. 1970 Apr 13;270(15):1947–1949. [PubMed] [Google Scholar]
  10. Kaplan H. B., Greenberg E. P. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol. 1985 Sep;163(3):1210–1214. doi: 10.1128/jb.163.3.1210-1214.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Makemson J. C. Control of in vivo luminescence in psychrophilic marine Photobacterium. Arch Mikrobiol. 1973 Nov 19;93(4):347–358. doi: 10.1007/BF00427930. [DOI] [PubMed] [Google Scholar]
  12. Mandel M., Higa A. Calcium-dependent bacteriophage DNA infection. J Mol Biol. 1970 Oct 14;53(1):159–162. doi: 10.1016/0022-2836(70)90051-3. [DOI] [PubMed] [Google Scholar]
  13. Nealson K. H. Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Arch Microbiol. 1977 Feb 4;112(1):73–79. doi: 10.1007/BF00446657. [DOI] [PubMed] [Google Scholar]
  14. Nealson K. H., Eberhard A., Hastings J. W. Catabolite repression of bacterial bioluminescence: functional implications. Proc Natl Acad Sci U S A. 1972 May;69(5):1073–1076. doi: 10.1073/pnas.69.5.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nealson K. H., Hastings J. W. Bacterial bioluminescence: its control and ecological significance. Microbiol Rev. 1979 Dec;43(4):496–518. doi: 10.1128/mr.43.4.496-518.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nealson K. H., Platt T., Hastings J. W. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol. 1970 Oct;104(1):313–322. doi: 10.1128/jb.104.1.313-322.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ogden S., Haggerty D., Stoner C. M., Kolodrubetz D., Schleif R. The Escherichia coli L-arabinose operon: binding sites of the regulatory proteins and a mechanism of positive and negative regulation. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3346–3350. doi: 10.1073/pnas.77.6.3346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Raibaud O., Schwartz M. Positive control of transcription initiation in bacteria. Annu Rev Genet. 1984;18:173–206. doi: 10.1146/annurev.ge.18.120184.001133. [DOI] [PubMed] [Google Scholar]
  19. Roy A., Danchin A. Restriction map of the cya region of the Escherichia coli K12 chromosome. Biochimie. 1981 Aug-Sep;63(8-9):719–722. doi: 10.1016/s0300-9084(81)80220-9. [DOI] [PubMed] [Google Scholar]
  20. Ruby E. G., Greenberg E. P., Hastings J. W. Planktonic marine luminous bacteria: species distribution in the water column. Appl Environ Microbiol. 1980 Feb;39(2):302–306. doi: 10.1128/aem.39.2.302-306.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ruby E. G., Nealson K. H. Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica; a model of symbiosis based on bacterial studies. Biol Bull. 1976 Dec;151(3):574–586. doi: 10.2307/1540507. [DOI] [PubMed] [Google Scholar]
  22. Sabourin D., Beckwith J. Deletion of the Escherichia coli crp gene. J Bacteriol. 1975 Apr;122(1):338–340. doi: 10.1128/jb.122.1.338-340.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schweizer H., Boos W. Transfer of the delta (argF-lac)U169 mutation between Escherichia coli strains by selection for a closely linked Tn10 insertion. Mol Gen Genet. 1983;192(1-2):293–294. doi: 10.1007/BF00327683. [DOI] [PubMed] [Google Scholar]
  24. Soll L., Berg P. Recessive lethals: a new class of nonsense suppressors in Escherichia coli. Proc Natl Acad Sci U S A. 1969 Jun;63(2):392–399. doi: 10.1073/pnas.63.2.392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ulitzur S., Yashphe J. An adenosine 3',5'-monophosphate-requiring mutant of the luminous bacteria Beneckea harveyi. Biochim Biophys Acta. 1975 Oct 9;404(2):321–328. doi: 10.1016/0304-4165(75)90339-6. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES