Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 May;86(10):3529–3533. doi: 10.1073/pnas.86.10.3529

Regulation of the iron uptake system in Vibrio anguillarum: evidence for a cooperative effect between two transcriptional activators.

P C Salinas 1, M E Tolmasky 1, J H Crosa 1
PMCID: PMC287171  PMID: 2542936

Abstract

We have identified a 110-kDa polypeptide that has a trans-acting regulatory activity on the expression of the pJM1 plasmid iron-uptake genes in Vibrio anguillarum. This protein is encoded by the angR gene and maps in a 3.6-kilobase-pair pJM1 DNA region located downstream of the iron transport genes. Full expression of this gene occurs under iron-limiting conditions and requires a 2.9-kilobase-pair upstream region in cis that maps within the coding region of the OM2 outer membrane protein, essential for the transport of iron into the cell cytosol. Determination of the siderophore anguibactin levels as well as analysis of specific transcripts for anguibactin biosynthetic genes demonstrated that AngR and another transcriptional activator, Taf, regulate in a synergistic fashion the level of anguibactin production by activation of transcription of the anguibactin biosynthetic genes under iron-limiting conditions.

Full text

PDF
3529

Images in this article

3532Image
on p.3532
3532Image
on p.3532
3533Image
on p.3533

Selected References

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

  1. Actis L. A., Fish W., Crosa J. H., Kellerman K., Ellenberger S. R., Hauser F. M., Sanders-Loehr J. Characterization of anguibactin, a novel siderophore from Vibrio anguillarum 775(pJM1). J Bacteriol. 1986 Jul;167(1):57–65. doi: 10.1128/jb.167.1.57-65.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Actis L. A., Potter S. A., Crosa J. H. Iron-regulated outer membrane protein OM2 of Vibrio anguillarum is encoded by virulence plasmid pJM1. J Bacteriol. 1985 Feb;161(2):736–742. doi: 10.1128/jb.161.2.736-742.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Actis L. A., Tolmasky M. E., Farrell D. H., Crosa J. H. Genetic and molecular characterization of essential components of the Vibrio anguillarum plasmid-mediated iron-transport system. J Biol Chem. 1988 Feb 25;263(6):2853–2860. [PubMed] [Google Scholar]
  4. Bagg A., Neilands J. B. Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry. 1987 Aug 25;26(17):5471–5477. doi: 10.1021/bi00391a039. [DOI] [PubMed] [Google Scholar]
  5. Belasco J. G., Beatty J. T., Adams C. W., von Gabain A., Cohen S. N. Differential expression of photosynthesis genes in R. capsulata results from segmental differences in stability within the polycistronic rxcA transcript. Cell. 1985 Jan;40(1):171–181. doi: 10.1016/0092-8674(85)90320-4. [DOI] [PubMed] [Google Scholar]
  6. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  7. Brosius J. Plasmid vectors for the selection of promoters. Gene. 1984 Feb;27(2):151–160. doi: 10.1016/0378-1119(84)90136-7. [DOI] [PubMed] [Google Scholar]
  8. Brosius J. Toxicity of an overproduced foreign gene product in Escherichia coli and its use in plasmid vectors for the selection of transcription terminators. Gene. 1984 Feb;27(2):161–172. doi: 10.1016/0378-1119(84)90137-9. [DOI] [PubMed] [Google Scholar]
  9. Bullen J. J., Rogers H. J., Griffiths E. Role of iron in bacterial infection. Curr Top Microbiol Immunol. 1978;80:1–35. doi: 10.1007/978-3-642-66956-9_1. [DOI] [PubMed] [Google Scholar]
  10. Crosa J. H. A plasmid associated with virulence in the marine fish pathogen Vibrio anguillarum specifies an iron-sequestering system. Nature. 1980 Apr 10;284(5756):566–568. doi: 10.1038/284566a0. [DOI] [PubMed] [Google Scholar]
  11. Crosa J. H., Hodges L. L., Schiewe M. H. Curing of a plasmid is correlated with an attenuation of virulence in the marine fish pathogen Vibrio anguillarum. Infect Immun. 1980 Mar;27(3):897–902. doi: 10.1128/iai.27.3.897-902.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Crosa J. H., Schiewe M. H., Falkow S. Evidence for plasmid contribution to the virulence of fish pathogen Vibrio anguillarum. Infect Immun. 1977 Nov;18(2):509–513. doi: 10.1128/iai.18.2.509-513.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Crosa J. H. The relationship of plasmid-mediated iron transport and bacterial virulence. Annu Rev Microbiol. 1984;38:69–89. doi: 10.1146/annurev.mi.38.100184.000441. [DOI] [PubMed] [Google Scholar]
  14. Figurski D. H., Helinski D. R. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648–1652. doi: 10.1073/pnas.76.4.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hantke K. Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12. Mol Gen Genet. 1984;197(2):337–341. doi: 10.1007/BF00330982. [DOI] [PubMed] [Google Scholar]
  16. Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet. 1981;182(2):288–292. doi: 10.1007/BF00269672. [DOI] [PubMed] [Google Scholar]
  17. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Neilands J. B. Microbial iron compounds. Annu Rev Biochem. 1981;50:715–731. doi: 10.1146/annurev.bi.50.070181.003435. [DOI] [PubMed] [Google Scholar]
  19. Prentki P., Krisch H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. doi: 10.1016/0378-1119(84)90059-3. [DOI] [PubMed] [Google Scholar]
  20. Prody C. A., Neilands J. B. Genetic and biochemical characterization of the Escherichia coli K-12 fhuB mutation. J Bacteriol. 1984 Mar;157(3):874–880. doi: 10.1128/jb.157.3.874-880.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
  22. Sancar A., Hack A. M., Rupp W. D. Simple method for identification of plasmid-coded proteins. J Bacteriol. 1979 Jan;137(1):692–693. doi: 10.1128/jb.137.1.692-693.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stachel S. E., An G., Flores C., Nester E. W. A Tn3 lacZ transposon for the random generation of beta-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. EMBO J. 1985 Apr;4(4):891–898. doi: 10.1002/j.1460-2075.1985.tb03715.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tolmasky M. E., Actis L. A., Crosa J. H. Genetic analysis of the iron uptake region of the Vibrio anguillarum plasmid pJM1: molecular cloning of genetic determinants encoding a novel trans activator of siderophore biosynthesis. J Bacteriol. 1988 Apr;170(4):1913–1919. doi: 10.1128/jb.170.4.1913-1919.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tolmasky M. E., Crosa J. H. Molecular cloning and expression of genetic determinants for the iron uptake system mediated by the Vibrio anguillarum plasmid pJM1. J Bacteriol. 1984 Dec;160(3):860–866. doi: 10.1128/jb.160.3.860-866.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tolmasky M. E., Salinas P. C., Actis L. A., Crosa J. H. Increased production of the siderophore anguibactin mediated by pJM1-like plasmids in Vibrio anguillarum. Infect Immun. 1988 Jun;56(6):1608–1614. doi: 10.1128/iai.56.6.1608-1614.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Walter M. A., Potter S. A., Crosa J. H. Iron uptake system medicated by Vibrio anguillarum plasmid pJM1. J Bacteriol. 1983 Nov;156(2):880–887. doi: 10.1128/jb.156.2.880-887.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Waters S. H., Rogowsky P., Grinsted J., Altenbuchner J., Schmitt R. The tetracycline resistance determinants of RP1 and Tn1721: nucleotide sequence analysis. Nucleic Acids Res. 1983 Sep 10;11(17):6089–6105. doi: 10.1093/nar/11.17.6089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weinberg E. D. Iron and infection. Microbiol Rev. 1978 Mar;42(1):45–66. doi: 10.1128/mr.42.1.45-66.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. de Boer H. A., Comstock L. J., Vasser M. The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc Natl Acad Sci U S A. 1983 Jan;80(1):21–25. doi: 10.1073/pnas.80.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. von Gabain A., Belasco J. G., Schottel J. L., Chang A. C., Cohen S. N. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc Natl Acad Sci U S A. 1983 Feb;80(3):653–657. doi: 10.1073/pnas.80.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES