Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Jan;177(1):252–258. doi: 10.1128/jb.177.1.252-258.1995

Nucleotide sequence of pvdD, a pyoverdine biosynthetic gene from Pseudomonas aeruginosa: PvdD has similarity to peptide synthetases.

T R Merriman 1, M E Merriman 1, I L Lamont 1
PMCID: PMC176582  PMID: 7798141

Abstract

Pseudomonas aeruginosa secretes a fluorescent siderophore, pyoverdine, when grown under iron-deficient conditions. Pyoverdine consists of a chromophoric group bound to a partly cyclic octapeptide. As a step toward understanding the molecular events involved in pyoverdine synthesis, we have sequenced a gene, pvdD, required for this process. The gene encodes a 2,448-residue protein, PvdD, which has a predicted molecular mass of 273,061 Da and contains two highly similar domains of about 1,000 amino acids each. The protein is similar to peptide synthetases from a range of bacterial and fungal species, indicating that synthesis of the peptide moiety of pyoverdine proceeds by a nonribosomal mechanism. The pvdD gene is adjacent to a gene, fpvA, which encodes an outer membrane receptor protein required for uptake of ferripyoverdine.

Full Text

The Full Text of this article is available as a PDF (472.9 KB).

Selected References

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

  1. Adams C., Dowling D. N., O'Sullivan D. J., O'Gara F. Isolation of a gene (pbsC) required for siderophore biosynthesis in fluorescent Pseudomonas sp. strain M114. Mol Gen Genet. 1994 Jun 3;243(5):515–524. doi: 10.1007/BF00284199. [DOI] [PubMed] [Google Scholar]
  2. Ankenbauer R., Sriyosachati S., Cox C. D. Effects of siderophores on the growth of Pseudomonas aeruginosa in human serum and transferrin. Infect Immun. 1985 Jul;49(1):132–140. doi: 10.1128/iai.49.1.132-140.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bankier A. T., Weston K. M., Barrell B. G. Random cloning and sequencing by the M13/dideoxynucleotide chain termination method. Methods Enzymol. 1987;155:51–93. doi: 10.1016/0076-6879(87)55009-1. [DOI] [PubMed] [Google Scholar]
  4. Bitter W., Marugg J. D., de Weger L. A., Tommassen J., Weisbeek P. J. The ferric-pseudobactin receptor PupA of Pseudomonas putida WCS358: homology to TonB-dependent Escherichia coli receptors and specificity of the protein. Mol Microbiol. 1991 Mar;5(3):647–655. doi: 10.1111/j.1365-2958.1991.tb00736.x. [DOI] [PubMed] [Google Scholar]
  5. Budzikiewicz H. Secondary metabolites from fluorescent pseudomonads. FEMS Microbiol Rev. 1993 Apr;10(3-4):209–228. doi: 10.1111/j.1574-6968.1993.tb05868.x. [DOI] [PubMed] [Google Scholar]
  6. Coque J. J., Martín J. F., Calzada J. G., Liras P. The cephamycin biosynthetic genes pcbAB, encoding a large multidomain peptide synthetase, and pcbC of Nocardia lactamdurans are clustered together in an organization different from the same genes in Acremonium chrysogenum and Penicillium chrysogenum. Mol Microbiol. 1991 May;5(5):1125–1133. doi: 10.1111/j.1365-2958.1991.tb01885.x. [DOI] [PubMed] [Google Scholar]
  7. Cornelis P., Hohnadel D., Meyer J. M. Evidence for different pyoverdine-mediated iron uptake systems among Pseudomonas aeruginosa strains. Infect Immun. 1989 Nov;57(11):3491–3497. doi: 10.1128/iai.57.11.3491-3497.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cosmina P., Rodriguez F., de Ferra F., Grandi G., Perego M., Venema G., van Sinderen D. Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis. Mol Microbiol. 1993 May;8(5):821–831. doi: 10.1111/j.1365-2958.1993.tb01629.x. [DOI] [PubMed] [Google Scholar]
  9. Cox C. D., Adams P. Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun. 1985 Apr;48(1):130–138. doi: 10.1128/iai.48.1.130-138.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. D'Souza C., Nakano M. M., Corbell N., Zuber P. Amino-acylation site mutations in amino acid-activating domains of surfactin synthetase: effects on surfactin production and competence development in Bacillus subtilis. J Bacteriol. 1993 Jun;175(11):3502–3510. doi: 10.1128/jb.175.11.3502-3510.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Farrell D. H., Mikesell P., Actis L. A., Crosa J. H. A regulatory gene, angR, of the iron uptake system of Vibrio anguillarum: similarity with phage P22 cro and regulation by iron. Gene. 1990 Jan 31;86(1):45–51. doi: 10.1016/0378-1119(90)90112-5. [DOI] [PubMed] [Google Scholar]
  13. Fuma S., Fujishima Y., Corbell N., D'Souza C., Nakano M. M., Zuber P., Yamane K. Nucleotide sequence of 5' portion of srfA that contains the region required for competence establishment in Bacillus subtilus. Nucleic Acids Res. 1993 Jan 11;21(1):93–97. doi: 10.1093/nar/21.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gocht M., Marahiel M. A. Analysis of core sequences in the D-Phe activating domain of the multifunctional peptide synthetase TycA by site-directed mutagenesis. J Bacteriol. 1994 May;176(9):2654–2662. doi: 10.1128/jb.176.9.2654-2662.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Guilvout I., Mercereau-Puijalon O., Bonnefoy S., Pugsley A. P., Carniel E. High-molecular-weight protein 2 of Yersinia enterocolitica is homologous to AngR of Vibrio anguillarum and belongs to a family of proteins involved in nonribosomal peptide synthesis. J Bacteriol. 1993 Sep;175(17):5488–5504. doi: 10.1128/jb.175.17.5488-5504.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gutiérrez S., Díez B., Montenegro E., Martín J. F. Characterization of the Cephalosporium acremonium pcbAB gene encoding alpha-aminoadipyl-cysteinyl-valine synthetase, a large multidomain peptide synthetase: linkage to the pcbC gene as a cluster of early cephalosporin biosynthetic genes and evidence of multiple functional domains. J Bacteriol. 1991 Apr;173(7):2354–2365. doi: 10.1128/jb.173.7.2354-2365.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Haas B., Kraut J., Marks J., Zanker S. C., Castignetti D. Siderophore presence in sputa of cystic fibrosis patients. Infect Immun. 1991 Nov;59(11):3997–4000. doi: 10.1128/iai.59.11.3997-4000.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haas B., Murphy E., Castignetti D. Siderophore synthesis by mucoid Pseudomonas aeruginosa strains isolated from cystic fibrosis patients. Can J Microbiol. 1991 Aug;37(8):654–657. doi: 10.1139/m91-111. [DOI] [PubMed] [Google Scholar]
  19. Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
  20. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kleinkauf H., von Döhren H. Nonribosomal biosynthesis of peptide antibiotics. Eur J Biochem. 1990 Aug 28;192(1):1–15. doi: 10.1111/j.1432-1033.1990.tb19188.x. [DOI] [PubMed] [Google Scholar]
  22. MacCabe A. P., van Liempt H., Palissa H., Unkles S. E., Riach M. B., Pfeifer E., von Döhren H., Kinghorn J. R. Delta-(L-alpha-aminoadipyl)-L-cysteinyl-D-valine synthetase from Aspergillus nidulans. Molecular characterization of the acvA gene encoding the first enzyme of the penicillin biosynthetic pathway. J Biol Chem. 1991 Jul 5;266(19):12646–12654. [PubMed] [Google Scholar]
  23. Magazin M. D., Moores J. C., Leong J. Cloning of the gene coding for the outer membrane receptor protein for ferric pseudobactin, a siderophore from a plant growth-promoting Pseudomonas strain. J Biol Chem. 1986 Jan 15;261(2):795–799. [PubMed] [Google Scholar]
  24. Moores J. C., Magazin M., Ditta G. S., Leong J. Cloning of genes involved in the biosynthesis of pseudobactin, a high-affinity iron transport agent of a plant growth-promoting Pseudomonas strain. J Bacteriol. 1984 Jan;157(1):53–58. doi: 10.1128/jb.157.1.53-58.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Morris J., O'sullivan D. J., Koster M., Leong J., Weisbeek P. J., O'gara F. Characterization of Fluorescent Siderophore-Mediated Iron Uptake in Pseudomonas sp. Strain M114: Evidence for the Existence of an Additional Ferric Siderophore Receptor. Appl Environ Microbiol. 1992 Feb;58(2):630–635. doi: 10.1128/aem.58.2.630-635.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Poole K., Neshat S., Krebes K., Heinrichs D. E. Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacteriol. 1993 Aug;175(15):4597–4604. doi: 10.1128/jb.175.15.4597-4604.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rusnak F., Sakaitani M., Drueckhammer D., Reichert J., Walsh C. T. Biosynthesis of the Escherichia coli siderophore enterobactin: sequence of the entF gene, expression and purification of EntF, and analysis of covalent phosphopantetheine. Biochemistry. 1991 Mar 19;30(11):2916–2927. doi: 10.1021/bi00225a027. [DOI] [PubMed] [Google Scholar]
  29. Saraste M., Sibbald P. R., Wittinghofer A. The P-loop--a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci. 1990 Nov;15(11):430–434. doi: 10.1016/0968-0004(90)90281-f. [DOI] [PubMed] [Google Scholar]
  30. Schlumbohm W., Stein T., Ullrich C., Vater J., Krause M., Marahiel M. A., Kruft V., Wittmann-Liebold B. An active serine is involved in covalent substrate amino acid binding at each reaction center of gramicidin S synthetase. J Biol Chem. 1991 Dec 5;266(34):23135–23141. [PubMed] [Google Scholar]
  31. Smith D. J., Earl A. J., Turner G. The multifunctional peptide synthetase performing the first step of penicillin biosynthesis in Penicillium chrysogenum is a 421,073 dalton protein similar to Bacillus brevis peptide antibiotic synthetases. EMBO J. 1990 Sep;9(9):2743–2750. doi: 10.1002/j.1460-2075.1990.tb07461.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sriyosachati S., Cox C. D. Siderophore-mediated iron acquisition from transferrin by Pseudomonas aeruginosa. Infect Immun. 1986 Jun;52(3):885–891. doi: 10.1128/iai.52.3.885-891.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Staab J. F., Elkins M. F., Earhart C. F. Nucleotide sequence of the Escherichia coli entE gene. FEMS Microbiol Lett. 1989 May;50(1-2):15–19. doi: 10.1016/0378-1097(89)90450-3. [DOI] [PubMed] [Google Scholar]
  34. Staden R. An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res. 1982 May 11;10(9):2951–2961. doi: 10.1093/nar/10.9.2951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Staden R., McLachlan A. D. Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res. 1982 Jan 11;10(1):141–156. doi: 10.1093/nar/10.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stockwell P. A. HOMED: a homologous sequence editor. Trends Biochem Sci. 1988 Aug;13(8):322–324. doi: 10.1016/0968-0004(88)90130-2. [DOI] [PubMed] [Google Scholar]
  37. Stockwell P. A. VTUTIN: a full screen gel management editor. Comput Appl Biosci. 1985 Dec;1(4):253–259. doi: 10.1093/bioinformatics/1.4.253. [DOI] [PubMed] [Google Scholar]
  38. Tolmasky M. E., Actis L. A., Crosa J. H. A single amino acid change in AngR, a protein encoded by pJM1-like virulence plasmids, results in hyperproduction of anguibactin. Infect Immun. 1993 Aug;61(8):3228–3233. doi: 10.1128/iai.61.8.3228-3233.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Turgay K., Krause M., Marahiel M. A. Four homologous domains in the primary structure of GrsB are related to domains in a superfamily of adenylate-forming enzymes. Mol Microbiol. 1992 Feb;6(4):529–546. doi: 10.1111/j.1365-2958.1992.tb01498.x. [DOI] [PubMed] [Google Scholar]
  40. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  41. Visca P., Ciervo A., Orsi N. Cloning and nucleotide sequence of the pvdA gene encoding the pyoverdin biosynthetic enzyme L-ornithine N5-oxygenase in Pseudomonas aeruginosa. J Bacteriol. 1994 Feb;176(4):1128–1140. doi: 10.1128/jb.176.4.1128-1140.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Weckermann R., Fürbass R., Marahiel M. A. Complete nucleotide sequence of the tycA gene coding the tyrocidine synthetase 1 from Bacillus brevis. Nucleic Acids Res. 1988 Dec 23;16(24):11841–11841. doi: 10.1093/nar/16.24.11841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. West S. E., Iglewski B. H. Codon usage in Pseudomonas aeruginosa. Nucleic Acids Res. 1988 Oct 11;16(19):9323–9335. doi: 10.1093/nar/16.19.9323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. von Döhren H. The organization of multifunctional peptide and depsipeptide synthetases. Biochem Soc Trans. 1993 Feb;21(1):214–217. doi: 10.1042/bst0210214. [DOI] [PubMed] [Google Scholar]

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

RESOURCES