• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of iaiPermissionsJournals.ASM.orgJournalIAI ArticleJournal InfoAuthorsReviewers
Infect Immun. Feb 1996; 64(2): 518–523.
PMCID: PMC173795

Pyoverdin is essential for virulence of Pseudomonas aeruginosa.

Abstract

The role of pyoverdin, the main siderophore in iron-gathering capacity produced by Pseudomonas aeruginosa, in bacterial growth in vivo is controversial, although iron is important for virulence. To determine the ability of pyoverdin to compete for iron with the human iron-binding protein transferrin, wild-type P. aeruginosa ATCC 15692 (PAO1 strain) and PAO pyoverdin-deficient mutants were grown at 37 degrees C in bicarbonate-containing succinate medium to which apotransferrin had been added. Growth of the pyoverdin-deficient mutants was fully inhibited compared with that of the wild type but was restored when pyoverdin was added to the medium. Moreover, when growth took place at a temperature at which no pyoverdin production occurred (43 degrees C), the wild-type PAO1 strain behaved the same as the pyoverdin-deficient mutants, with growth inhibited by apotransferrin in the presence of bicarbonate and restored by pyoverdin supplementation. Growth inhibition was never observed in bicarbonate-free succinate medium, whatever the strain and the temperature for growth. In vivo, in contrast to results obtained with the wild-type strain, pyoverdin-deficient mutants demonstrated no virulence when injected at 10(2) CFU into burned mice. However, virulence was restored when purified pyoverdin originating from the wild-type strain was supplemented during the infection. These results strongly suggest that pyoverdin competes directly with transferrin for iron and that it is an essential element for in vivo iron gathering and virulence expression in P. aeruginosa. Rapid removal of iron from [59Fe]ferritransferrin by pyoverdin in vitro supports this view.

Full Text

The Full Text of this article is available as a PDF (218K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ankenbauer R, Sriyosachati S, Cox CD. Effects of siderophores on the growth of Pseudomonas aeruginosa in human serum and transferrin. Infect Immun. 1985 Jul;49(1):132–140. [PMC free article] [PubMed]
  • Bjorn MJ, Sokol PA, Iglewski BH. Influence of iron on yields of extracellular products in Pseudomonas aeruginosa cultures. J Bacteriol. 1979 Apr;138(1):193–200. [PMC free article] [PubMed]
  • Bodey GP, Bolivar R, Fainstein V, Jadeja L. Infections caused by Pseudomonas aeruginosa. Rev Infect Dis. 1983 Mar-Apr;5(2):279–313. [PubMed]
  • Britigan BE, Hayek MB, Doebbeling BN, Fick RB., Jr Transferrin and lactoferrin undergo proteolytic cleavage in the Pseudomonas aeruginosa-infected lungs of patients with cystic fibrosis. Infect Immun. 1993 Dec;61(12):5049–5055. [PMC free article] [PubMed]
  • Cornelis P, Hohnadel D, Meyer JM. Evidence for different pyoverdine-mediated iron uptake systems among Pseudomonas aeruginosa strains. Infect Immun. 1989 Nov;57(11):3491–3497. [PMC free article] [PubMed]
  • Cornelis P, Moguilevsky N, Jacques JF, Masson PL. Study of the siderophores and receptors in different clinical isolates of Pseudomonas aeruginosa. Antibiot Chemother (1971) 1987;39:290–306. [PubMed]
  • Cox CD. Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol. 1980 May;142(2):581–587. [PMC free article] [PubMed]
  • Cox CD, Adams P. Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun. 1985 Apr;48(1):130–138. [PMC free article] [PubMed]
  • Daskaleros PA, Stoebner JA, Payne SM. Iron uptake in Plesiomonas shigelloides: cloning of the genes for the heme-iron uptake system. Infect Immun. 1991 Aug;59(8):2706–2711. [PMC free article] [PubMed]
  • Dean CR, Poole K. Cloning and characterization of the ferric enterobactin receptor gene (pfeA) of Pseudomonas aeruginosa. J Bacteriol. 1993 Jan;175(2):317–324. [PMC free article] [PubMed]
  • Döring G, Pfestorf M, Botzenhart K, Abdallah MA. Impact of proteases on iron uptake of Pseudomonas aeruginosa pyoverdin from transferrin and lactoferrin. Infect Immun. 1988 Jan;56(1):291–293. [PMC free article] [PubMed]
  • Fleiszig SM, Zaidi TS, Fletcher EL, Preston MJ, Pier GB. Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect Immun. 1994 Aug;62(8):3485–3493. [PMC free article] [PubMed]
  • Garibaldi JA. Influence of temperature on the iron metabolism of a fluorescent pseudomonad. J Bacteriol. 1971 Mar;105(3):1036–1038. [PMC free article] [PubMed]
  • Garibaldi JA. Influence of temperature on the biosynthesis of iron transport compounds by Salmonella typhimurium. J Bacteriol. 1972 Apr;110(1):262–265. [PMC free article] [PubMed]
  • Hallé F, Meyer JM. Ferrisiderophore reductases of Pseudomonas. Purification, properties and cellular location of the Pseudomonas aeruginosa ferripyoverdine reductase. Eur J Biochem. 1992 Oct 15;209(2):613–620. [PubMed]
  • Hallé F, Meyer JM. Iron release from ferrisiderophores. A multi-step mechanism involving a NADH/FMN oxidoreductase and a chemical reduction by FMNH2. Eur J Biochem. 1992 Oct 15;209(2):621–627. [PubMed]
  • Harding RA, Royt PW. Acquisition of iron from citrate by Pseudomonas aeruginosa. J Gen Microbiol. 1990 Sep;136(9):1859–1867. [PubMed]
  • Heinrichs DE, Young L, Poole K. Pyochelin-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular-mass outer membrane protein. Infect Immun. 1991 Oct;59(10):3680–3684. [PMC free article] [PubMed]
  • Hohnadel D, Meyer JM. Specificity of pyoverdine-mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol. 1988 Oct;170(10):4865–4873. [PMC free article] [PubMed]
  • Holloway BW, Römling U, Tümmler B. Genomic mapping of Pseudomonas aeruginosa PAO. Microbiology. 1994 Nov;140(Pt 11):2907–2929. [PubMed]
  • Konopka K, Bindereif A, Neilands JB. Aerobactin-mediated utilization of transferrin iron. Biochemistry. 1982 Dec 7;21(25):6503–6508. [PubMed]
  • Liu PV, Shokrani F. Biological activities of pyochelins: iron-chelating agents of Pseudomonas aeruginosa. Infect Immun. 1978 Dec;22(3):878–890. [PMC free article] [PubMed]
  • Massad G, Arceneaux JE, Byers BR. Acquisition of iron from host sources by mesophilic Aeromonas species. J Gen Microbiol. 1991 Feb;137(2):237–241. [PubMed]
  • Meyer JM. Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa: possible involvement of porin OprF in iron translocation. J Gen Microbiol. 1992 May;138(5):951–958. [PubMed]
  • Meyer JM, Hohnadel D, Hallé F. Cepabactin from Pseudomonas cepacia, a new type of siderophore. J Gen Microbiol. 1989 Jun;135(6):1479–1487. [PubMed]
  • Meyer JM, Hohnadel D, Khan A, Cornelis P. Pyoverdin-facilitated iron uptake in Pseudomonas aeruginosa: immunological characterization of the ferripyoverdin receptor. Mol Microbiol. 1990 Aug;4(8):1401–1405. [PubMed]
  • Pennington JE, Reynolds HY, Carbone PP. Pseudomonas pneumonia. A retrospective study of 36 cases. Am J Med. 1973 Aug;55(2):155–160. [PubMed]
  • Poole K, Young L, Neshat S. Enterobactin-mediated iron transport in Pseudomonas aeruginosa. J Bacteriol. 1990 Dec;172(12):6991–6996. [PMC free article] [PubMed]
  • Rella M, Mercenier A, Haas D. Transposon insertion mutagenesis of Pseudomonas aeruginosa with a Tn5 derivative: application to physical mapping of the arc gene cluster. Gene. 1985;33(3):293–303. [PubMed]
  • Schlabach MR, Bates GW. The synergistic binding of anions and Fe3+ by transferrin. Implications for the interlocking sites hypothesis. J Biol Chem. 1975 Mar 25;250(6):2182–2188. [PubMed]
  • Schryvers AB. Characterization of the human transferrin and lactoferrin receptors in Haemophilus influenzae. Mol Microbiol. 1988 Jul;2(4):467–472. [PubMed]
  • Schryvers AB, Morris LJ. Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol Microbiol. 1988 Mar;2(2):281–288. [PubMed]
  • Smith AW, Poyner DR, Hughes HK, Lambert PA. Siderophore activity of myo-inositol hexakisphosphate in Pseudomonas aeruginosa. J Bacteriol. 1994 Jun;176(12):3455–3459. [PMC free article] [PubMed]
  • Sokol PA, Ohman DE, Iglewski BH. A more sensitive plate assay for detection of protease production by Pseudomanas aeruginosa. J Clin Microbiol. 1979 Apr;9(4):538–540. [PMC free article] [PubMed]
  • Sriyosachati S, Cox CD. Siderophore-mediated iron acquisition from transferrin by Pseudomonas aeruginosa. Infect Immun. 1986 Jun;52(3):885–891. [PMC free article] [PubMed]
  • Stieritz DD, Holder IA. Experimental studies of the pathogenesis of infections due to Pseudomonas aeruginosa: description of a burned mouse model. J Infect Dis. 1975 Jun;131(6):688–691. [PubMed]
  • Stoebner JA, Payne SM. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect Immun. 1988 Nov;56(11):2891–2895. [PMC free article] [PubMed]
  • WARNER RC, WEBER I. The preparation of crystalline conalbumin. J Biol Chem. 1951 Jul;191(1):173–180. [PubMed]
  • Wolz C, Hohloch K, Ocaktan A, Poole K, Evans RW, Rochel N, Albrecht-Gary AM, Abdallah MA, Döring G. Iron release from transferrin by pyoverdin and elastase from Pseudomonas aeruginosa. Infect Immun. 1994 Sep;62(9):4021–4027. [PMC free article] [PubMed]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...