1887

Abstract

Under conditions of iron limitation, secretes a high-affinity siderophore pyoverdine to scavenge Fe(III) in the extracellular environment and shuttle it into the cell. Uptake of the pyoverdine–Fe(III) complex is mediated by a specific outer-membrane receptor protein, FpvA (ferripyoverdine receptor). Three siderovars can be distinguished, each producing a different pyoverdine (type I–III) and a cognate FpvA receptor. Growth of an mutant of PAO1 (type I) under iron-limiting conditions can still be stimulated by its cognate pyoverdine, suggesting the presence of an alternative uptake route for type I ferripyoverdine. analysis of the PAO1 genome revealed that the product of gene PA4168 has a high similarity with FpvA. Inactivation of PA4168 (termed ) in an mutant totally abolished the capacity to utilize type I pyoverdine. The expression of is induced by iron limitation in Casamino acids (CAA) and in M9-glucose medium, but, unlike , not in a complex deferrated medium containing glycerol as carbon source. The gene was also detected in other isolates, including strains producing type II and type III pyoverdines. Inactivation of the homologues in these strains impaired their capacity to utilize type I ferripyoverdine as a source of iron. Accordingly, introduction of restored the capacity to utilize type I ferripyoverdine.

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2004-06-01
2024-04-18
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References

  1. Barton H. A., Johnson Z., Cox C. D., Vasil A. I., Vasil M. L. 1996; Ferric uptake regulator mutants of Pseudomonas aeruginosa with distinct alterations in the iron-dependent repression of exotoxin A and siderophores in aerobic and microaerobic environments. Mol Microbiol 21:1001–1017 [CrossRef]
    [Google Scholar]
  2. Baysse C., Meyer J. M., Plesiat P., Geoffroy V., Michel-Briand Y., Cornelis P. 1999; Uptake of pyocin S3 occurs through the outer membrane ferripyoverdine type II receptor of Pseudomonas aeruginosa. J Bacteriol 181:3849–3851
    [Google Scholar]
  3. Beare P. A., For R. J., Martin L., Lamont I. L. 2003; Siderophore mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol Microbiol 47:195–207
    [Google Scholar]
  4. Bolivar F. 1978; Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique EcoRI-generated recombinant DNA molecules. Gene 4:121–136 [CrossRef]
    [Google Scholar]
  5. Budzikiewicz H. 1993; Secondary metabolites from fluorescent pseudomonads. FEMS Microbiol Rev 104:209–228 [CrossRef]
    [Google Scholar]
  6. Cornelis P., Matthijs S. 2002; Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 4:787–798 [CrossRef]
    [Google Scholar]
  7. Cornelis P., Hohnadel D., Meyer J. M. 1989; Evidence for different pyoverdine-mediated iron uptake systems among Pseudomonas aeruginosa strains. Infect Immun 57:3491–3497
    [Google Scholar]
  8. Cornelis P., Anjaiah V., Koedam N., Delfosse P., Jacques P., Thonart P., Neirinckx L. 1992; Stability, frequency and multiplicity of transposon insertions in the pyoverdine region in the chromosomes of different fluorescent pseudomonads. J Gen Microbiol 138:1337–1343 [CrossRef]
    [Google Scholar]
  9. De Chial M., Ghysels B., Beatson S. A.9 other authors 2003; Identification of type II and type III pyoverdine receptors from Pseudomonas aeruginosa. Microbiology 149:821–831 [CrossRef]
    [Google Scholar]
  10. de Lorenzo V., Herrero M., Jakubzik U., Timmis K. N. 1990; Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172:6568–6572
    [Google Scholar]
  11. Dennis J. J., Zylstra G. J. 1998; Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 64:2710–2715
    [Google Scholar]
  12. De Vos D., Lim A. Jr, Pirnay J. P., Struelens M., Vandevelde C., Duinslaeger L., Vanderkelen A., Cornelis P. 2001; Study of pyoverdine type and Pseudomonas aeruginosa isolated from cystic fibrosis patients: prevalence of type II pyoverdine isolates and accumulation of pyoverdine-negative mutations. Arch Microbiol 175:384–388 [CrossRef]
    [Google Scholar]
  13. Ernst R. K., D'Argenio D. A., Ichikawa J. K.12 other authors 2003; Genome mosaicism is conserved but not unique in Pseudomonas aeruginosa isolates from the airways of young children with cystic fibrosis. Environ Microbiol 5:1341–1349 [CrossRef]
    [Google Scholar]
  14. Ferguson A. D., Hofmann E., Coulton J. W., Diederichs K., Welte W. 1998; Siderophore-mediated iron transport: crystal structure FhuA with bound lipopolysaccharide. Science 282:2215–2220 [CrossRef]
    [Google Scholar]
  15. Guerinot M. L. 1994; Microbial iron transport. Annu Rev Microbiol 48:743–772 [CrossRef]
    [Google Scholar]
  16. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
    [Google Scholar]
  17. Heim S., Ferrer M., Heuer H., Regenhardt D., Nimtz M., Timmis K. N. 2003; Proteome reference map of Pseudomonas putida strain KT2440 for genome expression profiling: distinct responses of KT2440 and Pseudomonas aeruginosa strain PAO1 to iron deprivation and a new form of superoxide dismutase. Environ Microbiol 5:1257–1269 [CrossRef]
    [Google Scholar]
  18. Herrero M., Timmis K. N., de Lorenzo V. 1990; Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram negative bacteria. J Bacteriol 172:6557–6567
    [Google Scholar]
  19. Hoang T. T., Karkhoff-Schweizer R. R., Kutchma A. J., Schweizer H. P. 1998; A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77–86 [CrossRef]
    [Google Scholar]
  20. Höfte M., Mergeay M., Verstraete W. 1990; Marking the rhizopseudomonas strain 7NSK2 with a Mu Δ(lac) element for ecological studies. Appl Environ Microbiol 56:1046–1052
    [Google Scholar]
  21. Höfte M., Buysens S., Koedam N., Cornelis P. 1993; Zinc affects siderophore-mediated high affinity iron uptake systems in the rizosphere Pseudomonas aeruginosa 7NSK2. Bio/Metals 6:85–91
    [Google Scholar]
  22. Holloway B. 1955; Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13:572–581 [CrossRef]
    [Google Scholar]
  23. Koebnik R., Locher K. P., Van Gelder P. 2000; Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253 [CrossRef]
    [Google Scholar]
  24. Koster M., Leong J., Weisbeek P. J., van de Vossenberg J. 1993; Identification and characterization of the pupB gene encoding an inducible ferric-pseudobactin receptor ofPseudomonas putida WCS358. Mol Microbiol 8:591–601 [CrossRef]
    [Google Scholar]
  25. Kovach M. E., Phillips R. W., Elzer P. H., Roop R. M., Peterson K. M. 1994; pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16:800–802
    [Google Scholar]
  26. Lamont I. L., Martin L. W. 2003; Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology 149:833–842 [CrossRef]
    [Google Scholar]
  27. Lamont I. L., Beare P. A., Ochsner U., Vasil A. I., Vasil M. L. 2002; Siderophore mediated signalling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 99:7072–7077 [CrossRef]
    [Google Scholar]
  28. Lehoux D. E., Sanschagrin F., Levesque R. C. 2000; Genomics of the 35-kb pvd locus and analysis of novel pvdIJK genes implicated in pyoverdine biosynthesis inPseudomonas aeruginosa. FEMS Microbiol Lett 190:141–146 [CrossRef]
    [Google Scholar]
  29. Lim A., Jr, De Vos D., Brauns M., Mossialos D., Gaballa A., Qing D., Cornelis P. 1997; Molecular and immunological characterisation of OprL, the 18 KDa outer-membrane peptidoglycan-associated lipoprotein (PAL) of Pseudomonas aeruginosa. Microbiology 143:1709–1716 [CrossRef]
    [Google Scholar]
  30. Meyer J. M., Abdallah M. A. 1978; The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physico-chemical properties. J Gen Microbiol 107:319–328 [CrossRef]
    [Google Scholar]
  31. Meyer J. M., Neely A., Stintzi A., Georges C., Holder I. A. 1996; Pyoverdine is essential for virulence of Pseudomonas aeruginosa. Infect Immun 64:518–523
    [Google Scholar]
  32. Meyer J. M., Stintzi A., De Vos D., Cornelis P., Tappe R., Taraz K., Budzikiewicz H. 1997; Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143:35–43 [CrossRef]
    [Google Scholar]
  33. Meyer J. M., Geoffroy V. A., Baida N., Gardan L., Izard D., Lemanceau P., Achouak W., Palleroni N. J. 2002a; Siderophore typing, a powerful tool for the identification of fluorescent and nonfluorescent pseudomonads. Appl Environ Microbiol 68:2745–2753 [CrossRef]
    [Google Scholar]
  34. Meyer J. M., Geoffroy V., Baysse C., Cornelis P., Barelmann I., Taraz K., Budzikiewicz H. 2002b; Siderophore mediated iron uptake in fluorescent Pseudomonas: characterization of the pyoverdine-receptor binding site of three cross-reacting pyoverdines. Arch Biochem Biophys 397:179–183 [CrossRef]
    [Google Scholar]
  35. Mizuno T., Kageyama M. 1978; Separation and characterization of the outer membrane of Pseudomonas aeruginosa. J Biochem 84:179–191
    [Google Scholar]
  36. Morris J., Donnelly D. F., O'Neill E., McConnell F., O'Gara F. 1994; Nucleotide sequence analysis and potential environmental distribution of a ferric pseudobactin receptor gene of Pseudomonassp. strain M114. Mol Gen Genet 242:9–16
    [Google Scholar]
  37. Ochsner U. A., Johnson Z., Lamont I. L., Cunliffe H. E., Vasil M. L. 1996; Exotoxin A production in Pseudomonas aeruginosa requires the iron-regulated pvdS gene encoding an alternative sigma factor. Mol Microbiol 21:1019–1028 [CrossRef]
    [Google Scholar]
  38. Ochsner U. A., Wilderman P. J., Vasil A. I., Vasil M. L. 2002; GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45:1277–1287 [CrossRef]
    [Google Scholar]
  39. Palma M., Worgall S., Quadri L. E. N. 2003; Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch Microbiol 180:374–379 [CrossRef]
    [Google Scholar]
  40. Pattery T., Hernalsteens J. P., De Greve H. 1999; Identification and molecular characterization of a novel Salmonella enteritidis pathogenicity islet encoding an ABC transporter. Mol Microbiol 33:791–805 [CrossRef]
    [Google Scholar]
  41. Pirnay J. P., De Vos D., Cochez C., Biloq F., Vanderkelen A., Zizi M., Ghysels B., Cornelis P. 2002; Pseudomonas aeruginosa displays an epidemic population structure. Environ Microbiol 4:898–911 [CrossRef]
    [Google Scholar]
  42. Poole K., McKay G. A. 2003; Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front Biosc 8:661–686 [CrossRef]
    [Google Scholar]
  43. Poole K., Neshat S., Krebes K., Heinrichs D. E. 1993; Cloning and nucleotide sequence of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacteriol 175:4597–4604
    [Google Scholar]
  44. Ratledge C., Dover L. G. 2000; Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941 [CrossRef]
    [Google Scholar]
  45. Ravel J., Cornelis P. 2003; Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11:195–200 [CrossRef]
    [Google Scholar]
  46. Schalk I. J., Hennard H., Dugave C., Poole K., Abdallah M. A., Pattus F. 2001; Iron-free pyoverdine binds to its outer membrane FpvA in Pseudomonas aeruginosa: a new mechanism for membrane iron transport. Mol Microbiol 39:351–360 [CrossRef]
    [Google Scholar]
  47. Schalk I. J., Abdallah M. A., Pattus F. 2002; Recycling of pyoverdin on the FpvA receptor after ferric pyoverdine uptake and dissociation in Pseudomonas aeruginosa. Biochemistry 41:1663–1671 [CrossRef]
    [Google Scholar]
  48. Shen J., Meldrum A., Poole K. 2002; FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa. J Bacteriol 184:3268–3275 [CrossRef]
    [Google Scholar]
  49. Smith A. W., Hirst P. H., Hughes K., Gensberg K., Govan J. R. 1992; The pyocin Sa receptor of Pseudomonas aeruginosa is associated with ferripyoverdin uptake. J Bacteriol 174:4847–4849
    [Google Scholar]
  50. Spencer D. H., Kas A., Smith E. E., Raymond C. K., Sims E. H., Hastings M., Burns J. L., Kaul R., Olson M. V. 2003; Whole-genome sequence variation among multiple isolates of Pseudomonas aeruginosa. J Bacteriol 185:1316–1325 [CrossRef]
    [Google Scholar]
  51. Stover C. K., Pham X. O., Erwin A. L.28 other authors 2000; Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964 [CrossRef]
    [Google Scholar]
  52. Takase H., Nitanai H., Hoshino K., Otani T. 2000; Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect Immun 68:1834–1839 [CrossRef]
    [Google Scholar]
  53. Van Haute E., Joos H., Maes M., Warren G., Van Montagu M., Schell J. 1983; Intergeneric transfer and exchange recombination of restriction fragments cloned in pBR322: a novel strategy for the reversed genetics of the Ti plasmids of Agrobacterium tumefaciens. EMBO J 2:411–417
    [Google Scholar]
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