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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27035-0
2004-06-01
2020-04-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/6/mic1501671.html?itemId=/content/journal/micro/10.1099/mic.0.27035-0&mimeType=html&fmt=ahah

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 Microbiol21:1001–1017[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 Bacteriol181:3849–3851
    [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 Microbiol47:195–207
    [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. Gene4:121–136[CrossRef]
    [Google Scholar]
  5. Budzikiewicz H.. 1993; Secondary metabolites from fluorescent pseudomonads. FEMS Microbiol Rev104:209–228[CrossRef]
    [Google Scholar]
  6. Cornelis P., Matthijs S.. 2002; Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol4:787–798[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 Immun57:3491–3497
    [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 Microbiol138:1337–1343[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. Microbiology149:821–831[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 Bacteriol172:6568–6572
    [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 Microbiol64:2710–2715
    [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 Microbiol175:384–388[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 Microbiol5:1341–1349[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. Science282:2215–2220[CrossRef]
    [Google Scholar]
  15. Guerinot M. L.. 1994; Microbial iron transport. Annu Rev Microbiol48:743–772[CrossRef]
    [Google Scholar]
  16. Hanahan D.. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580[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 Microbiol5:1257–1269[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 Bacteriol172:6557–6567
    [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. Gene212:77–86[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 Microbiol56:1046–1052
    [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/Metals6:85–91
    [Google Scholar]
  22. Holloway B.. 1955; Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol13:572–581[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 Microbiol37:239–253[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 Microbiol8:591–601[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. Biotechniques16:800–802
    [Google Scholar]
  26. Lamont I. L., Martin L. W.. 2003; Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology149:833–842[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 A99:7072–7077[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 Lett190:141–146[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. Microbiology143:1709–1716[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 Microbiol107:319–328[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 Immun64:518–523
    [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. Microbiology143:35–43[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 Microbiol68:2745–2753[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 Biophys397:179–183[CrossRef]
    [Google Scholar]
  35. Mizuno T., Kageyama M.. 1978; Separation and characterization of the outer membrane of Pseudomonas aeruginosa. J Biochem84:179–191
    [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 Genet242:9–16
    [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 Microbiol21:1019–1028[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 Microbiol45:1277–1287[CrossRef]
    [Google Scholar]
  39. Palma M., Worgall S., Quadri L. E. N.. 2003; Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch Microbiol180:374–379[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 Microbiol33:791–805[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 Microbiol4:898–911[CrossRef]
    [Google Scholar]
  42. Poole K., McKay G. A.. 2003; Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front Biosc8:661–686[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 Bacteriol175:4597–4604
    [Google Scholar]
  44. Ratledge C., Dover L. G.. 2000; Iron metabolism in pathogenic bacteria. Annu Rev Microbiol54:881–941[CrossRef]
    [Google Scholar]
  45. Ravel J., Cornelis P.. 2003; Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol11:195–200[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 Microbiol39:351–360[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. Biochemistry41:1663–1671[CrossRef]
    [Google Scholar]
  48. Shen J., Meldrum A., Poole K.. 2002; FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa. J Bacteriol184:3268–3275[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 Bacteriol174:4847–4849
    [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 Bacteriol185:1316–1325[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. Nature406:959–964[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 Immun68:1834–1839[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 J2:411–417
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27035-0
Loading
/content/journal/micro/10.1099/mic.0.27035-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error