Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 Dec;172(12):6991–6996. doi: 10.1128/jb.172.12.6991-6996.1990

Enterobactin-mediated iron transport in Pseudomonas aeruginosa.

K Poole 1, L Young 1, S Neshat 1
PMCID: PMC210819  PMID: 2174865

Abstract

A pyoverdine-deficient strain of Pseudomonas aeruginosa was unable to grow in an iron-deficient minimal medium in the presence of the nonmetabolizable iron chelator ethylene diamine-di(omega-hydroxyphenol acetic acid) (EDDHA), although addition of enterobactin to EDDHA-containing minimal media did restore growth of the pyoverdine-deficient P. aeruginosa. Consistent with the apparent ability of enterobactin to provide iron to P. aeruginosa, enterobactin-dependent 55Fe3+ uptake was observed in cells of P. aeruginosa previously grown in an iron-deficient medium containing enterobactin (or enterobactin-containing Escherichia coli culture supernatant). This uptake was energy dependent, was observable at low concentrations (60 nM) of FeCl3, and was absent in cells cultured without enterobactin. A novel protein with a molecular weight of approximately 80,000 was identified in the outer membranes of cells grown in iron-deficient minimal medium containing enterobactin, concomitant with the induction of enterobactin-dependent iron uptake. A Tn501 insertion mutant lacking this protein was isolated and shown to be deficient in enterobactin-mediated iron transport at 60 nM FeCl3, although it still exhibited enterobactin-dependent growth in iron-deficient medium containing EDDHA. It was subsequently observed that the mutant was, however, capable of enterobactin-mediated iron transport at much higher concentrations (600 nM) of FeCl3. Indeed, enterobactin-dependent iron uptake at this concentration of iron was observed in both the mutant and parent strains irrespective of whether they had been cultured in the presence of enterobactin.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
6991

Images in this article

Selected References

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

  1. Ankenbauer R., Hanne L. F., Cox C. D. Mapping of mutations in Pseudomonas aeruginosa defective in pyoverdin production. J Bacteriol. 1986 Jul;167(1):7–11. doi: 10.1128/jb.167.1.7-11.1986. [DOI] [PMC free article] [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. Benjamin W. H., Jr, Turnbough C. L., Jr, Posey B. S., Briles D. E. The ability of Salmonella typhimurium to produce the siderophore enterobactin is not a virulence factor in mouse typhoid. Infect Immun. 1985 Nov;50(2):392–397. doi: 10.1128/iai.50.2.392-397.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Botzenhart K., Rüden H. Hospital infections caused by Pseudomonas aeruginosa. Antibiot Chemother (1971) 1987;39:1–15. doi: 10.1159/000414328. [DOI] [PubMed] [Google Scholar]
  5. Cornelis P., Moguilevsky N., Jacques J. F., Masson P. L. Study of the siderophores and receptors in different clinical isolates of Pseudomonas aeruginosa. Antibiot Chemother (1971) 1987;39:290–306. doi: 10.1159/000414354. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Cox C. D. Effect of pyochelin on the virulence of Pseudomonas aeruginosa. Infect Immun. 1982 Apr;36(1):17–23. doi: 10.1128/iai.36.1.17-23.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cox C. D. Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol. 1980 May;142(2):581–587. doi: 10.1128/jb.142.2.581-587.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Frost G. E., Rosenberg H. The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim Biophys Acta. 1973 Nov 30;330(1):90–101. doi: 10.1016/0005-2736(73)90287-3. [DOI] [PubMed] [Google Scholar]
  11. Gilleland H. E., Jr, Stinnett J. D., Eagon R. G. Ultrastructural and chemical alteration of the cell envelope of Pseudomonas aeruginosa, associated with resistance to ethylenediaminetetraacetate resulting from growth in a Mg2+-deficient medium. J Bacteriol. 1974 Jan;117(1):302–311. doi: 10.1128/jb.117.1.302-311.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Griffiths E., Humphreys J. Isolation of enterochelin from the peritoneal washings of guinea pigs lethally infected with Escherichia coli. Infect Immun. 1980 Apr;28(1):286–289. doi: 10.1128/iai.28.1.286-289.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hancock R. E., Hantke K., Braun V. Iron transport in Escherichia coli K-12. 2,3-Dihydroxybenzoate-promoted iron uptake. Arch Microbiol. 1977 Sep 28;114(3):231–239. doi: 10.1007/BF00446867. [DOI] [PubMed] [Google Scholar]
  14. Hancock R. E., Hantke K., Braun V. Iron transport of Escherichia coli K-12: involvement of the colicin B receptor and of a citrate-inducible protein. J Bacteriol. 1976 Sep;127(3):1370–1375. doi: 10.1128/jb.127.3.1370-1375.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hantke K., Braun V. Membrane receptor dependent iron transport in Escherichia coli. FEBS Lett. 1975 Jan 1;49(3):301–305. doi: 10.1016/0014-5793(75)80771-x. [DOI] [PubMed] [Google Scholar]
  16. Hantke K. Dihydroxybenzoylserine--a siderophore for E. coli. FEMS Microbiol Lett. 1990 Jan 15;55(1-2):5–8. doi: 10.1016/0378-1097(90)90158-m. [DOI] [PubMed] [Google Scholar]
  17. Hantke K. Identification of an iron uptake system specific for coprogen and rhodotorulic acid in Escherichia coli K12. Mol Gen Genet. 1983;191(2):301–306. doi: 10.1007/BF00334830. [DOI] [PubMed] [Google Scholar]
  18. Hohnadel D., Meyer J. M. Specificity of pyoverdine-mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol. 1988 Oct;170(10):4865–4873. doi: 10.1128/jb.170.10.4865-4873.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ichihara S., Mizushima S. Identification of an outer membrane protein responsible for the binding of the Fe-enterochelin complex to Escherichia coli cells. J Biochem. 1978 Jan;83(1):137–140. doi: 10.1093/oxfordjournals.jbchem.a131884. [DOI] [PubMed] [Google Scholar]
  20. Jones R. L., Peterson C. M., Grady R. W., Kumbaraci T., Cerami A., Graziano J. H. Effects of iron chelators and iron overload on Salmonella infection. Nature. 1977 May 5;267(5606):63–65. doi: 10.1038/267063a0. [DOI] [PubMed] [Google Scholar]
  21. Khimji P. L., Miles A. A. Microbial iron-chelators and their action on Klebsiella infections in the skin of guinea-pigs. Br J Exp Pathol. 1978 Apr;59(2):137–147. [PMC free article] [PubMed] [Google Scholar]
  22. Konopka K., Bindereif A., Neilands J. B. Aerobactin-mediated utilization of transferrin iron. Biochemistry. 1982 Dec 7;21(25):6503–6508. doi: 10.1021/bi00268a028. [DOI] [PubMed] [Google Scholar]
  23. Langman L., Young I. G., Frost G. E., Rosenberg H., Gibson F. Enterochelin system of iron transport in Escherichia coli: mutations affecting ferric-enterochelin esterase. J Bacteriol. 1972 Dec;112(3):1142–1149. doi: 10.1128/jb.112.3.1142-1149.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Liu P. V., Shokrani F. Biological activities of pyochelins: iron-chelating agents of Pseudomonas aeruginosa. Infect Immun. 1978 Dec;22(3):878–890. doi: 10.1128/iai.22.3.878-890.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lugtenberg B., Meijers J., Peters R., van der Hoek P., van Alphen L. Electrophoretic resolution of the "major outer membrane protein" of Escherichia coli K12 into four bands. FEBS Lett. 1975 Oct 15;58(1):254–258. doi: 10.1016/0014-5793(75)80272-9. [DOI] [PubMed] [Google Scholar]
  26. Montgomerie J. Z. Epidemiology of Klebsiella and hospital-associated infections. Rev Infect Dis. 1979 Sep-Oct;1(5):736–753. doi: 10.1093/clinids/1.5.736. [DOI] [PubMed] [Google Scholar]
  27. Neilands J. B. Iron absorption and transport in microorganisms. Annu Rev Nutr. 1981;1:27–46. doi: 10.1146/annurev.nu.01.070181.000331. [DOI] [PubMed] [Google Scholar]
  28. Ninnemann J. L. Clinical and immune status of burn patients. Antibiot Chemother (1971) 1987;39:16–25. doi: 10.1159/000414330. [DOI] [PubMed] [Google Scholar]
  29. O'Brien I. G., Gibson F. The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli. Biochim Biophys Acta. 1970 Aug 14;215(2):393–402. doi: 10.1016/0304-4165(70)90038-3. [DOI] [PubMed] [Google Scholar]
  30. Payne S. M., Niesel D. W., Peixotto S. S., Lawlor K. M. Expression of hydroxamate and phenolate siderophores by Shigella flexneri. J Bacteriol. 1983 Sep;155(3):949–955. doi: 10.1128/jb.155.3.949-955.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Poole K., Hancock R. E. Isolation of a Tn501 insertion mutant lacking porin protein P of Pseudomonas aeruginosa. Mol Gen Genet. 1986 Mar;202(3):403–409. doi: 10.1007/BF00333269. [DOI] [PubMed] [Google Scholar]
  32. Rogers H. J. Iron-Binding Catechols and Virulence in Escherichia coli. Infect Immun. 1973 Mar;7(3):445–456. doi: 10.1128/iai.7.3.445-456.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schnaitman C. A. Outer membrane proteins of Escherichia coli. 3. Evidence that the major protein of Escherichia coli O111 outer membrane consists of four distinct polypeptide species. J Bacteriol. 1974 May;118(2):442–453. doi: 10.1128/jb.118.2.442-453.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sokol P. A. Production and utilization of pyochelin by clinical isolates of Pseudomonas cepacia. J Clin Microbiol. 1986 Mar;23(3):560–562. doi: 10.1128/jcm.23.3.560-562.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Tsuda M., Harayama S., Iino T. Tn501 insertion mutagenesis in Pseudomonas aeruginosa PAO. Mol Gen Genet. 1984;196(3):494–500. doi: 10.1007/BF00436198. [DOI] [PubMed] [Google Scholar]
  37. Warner P. J., Williams P. H., Bindereif A., Neilands J. B. ColV plasmid-specific aerobactin synthesis by invasive strains of Escherichia coli. Infect Immun. 1981 Aug;33(2):540–545. doi: 10.1128/iai.33.2.540-545.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weinberg E. D. Iron withholding: a defense against infection and neoplasia. Physiol Rev. 1984 Jan;64(1):65–102. doi: 10.1152/physrev.1984.64.1.65. [DOI] [PubMed] [Google Scholar]
  39. Yancey R. J., Breeding S. A., Lankford C. E. Enterochelin (enterobactin): virulence factor for Salmonella typhimurium. Infect Immun. 1979 Apr;24(1):174–180. doi: 10.1128/iai.24.1.174-180.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES