1887

Abstract

produces, under conditions of iron limitation, a high-affinity siderophore, pyoverdine (PVD), which is recognized at the level of the outer membrane by a specific TonB-dependent receptor, FpvA. So far, for , three different PVDs, differing in their peptide chain, have been described (types I–III), but only the FpvA receptor for type I is known. Two PVD-producing strains, one type II and one type III, were mutagenized by a mini-Tn transposon. In each case, one mutant unable to grow in the presence of the strong iron chelator ethylenediaminedihydroxyphenylacetic acid (EDDHA) and the cognate PVD was selected. The first mutant, which had an insertion in the gene, upstream of , was unable to take up type II PVD and showed resistance to pyocin S3, which is known to use type II FpvA as receptor. The second mutant was unable to take up type III PVD and had the transposon insertion in . Cosmid libraries of the respective type II and type III PVD wild-type strains were constructed and screened for clones restoring the capacity to grow in the presence of PVD. From the respective complementing genomic fragments, type II and type III sequences were determined. When , type II and type III restored PVD production, uptake, growth in the presence of EDDHA and, in the case of type II , pyocin S3 sensitivity. Complementation of mutants obtained by allelic exchange was achieved by the presence of cognate . All three receptors posses an N-terminal extension of about 70 amino acids, similar to FecA of , but only FpvAI has a TAT export sequence at its N-terminal end.

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2003-04-01
2020-09-28
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References

  1. Al-Samarrai T. H., Zhang N., Lamont I. L., Martin L., Kolbe J., Wilsher M., Morris A. J., Schmid J.. 2000; Simple and inexpensive but highly discriminating method for computer-assisted DNA fingerprinting of Pseudomonas aeruginosa . J Clin Microbiol38:4445–4452
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402
    [Google Scholar]
  3. 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]
  4. Baysse C., Matthijs S., Pattery T., Cornelis P.. 2001; Impact of mutations in hemA and hemH genes on pyoverdine production by Pseudomonas fluorescens ATCC17400. FEMS Microbiol Lett205:57–63
    [Google Scholar]
  5. Baysse C., Budzikiewicz H., Uria-Fernandez D., Cornelis P.. 2002; Impaired maturation of the siderophore pyoverdine chromophore in Pseudomonas fluorescens ATCC 17400 deficient for the cytochrome c biogenesis protein CcmC. FEBS Lett523:23–28
    [Google Scholar]
  6. Bodey G. P., Bolivar R., Fainstein V., Jadeja L.. 1983; Infections caused by Pseudomonas aeruginosa . Rev Infect Dis5:279–313
    [Google Scholar]
  7. Bolivar F.. 1978; Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique Eco RI sites for selection of Eco RI-generated recombinant DNA molecules. Gene4:121–136
    [Google Scholar]
  8. Boyer H. W., Roulland-Dussoix D.. 1969; A complementation analysis of the restriction and modification of DNA in Escherichia coli . J Mol Biol41:459–472
    [Google Scholar]
  9. Cheng K., Smyth R. L., Govan J. R., Doherty C., Winstanley C., Denning N., Heaf D. P., van Saene H., Hart C. A.. 1996; Spread of beta-lactam-resistant Pseudomonas aeruginosa in a cystic fibrosis clinic. Lancet348:639–642
    [Google Scholar]
  10. 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]
  11. 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
    [Google Scholar]
  12. de Lorenzo V., Herrero M., Jakubzik U., Timmis K. N.. 1990; Mini-Tn 5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol172:6568–6572
    [Google Scholar]
  13. De Vos D., Lim A. Jr, Pirnay J. P., Struelens M., Vandevelde C., Duinslaeger L., Vanderkelen A., Cornelis P.. 1997; Direct detection and identification of Pseudomonas aeruginosa in clinical samples such as skin biopsy specimens and expectorations by multiplex PCR based on two outer membrane liporotein genes,oprI and oprL . J Clin Microbiol35:1295–1299
    [Google Scholar]
  14. De Vos D., De Chial M., Cochez C., Jansen S., Tummler B., Meyer J. M., Cornelis P.. 2001; Study of pyoverdine type and production by Pseudomonas aeruginosa isolated from cystic fibrosis patients: prevalence of type II pyoverdine isolates and accumulation of pyoverdine-negative mutations. Arch Microbiol175:384–388
    [Google Scholar]
  15. Duport C., Baysse C., Michel-Briand Y.. 1995; Molecular characterization of pyocin S3, a novel S-type pyocin from Pseudomonas aeruginosa . J Biol Chem270:8920–8927
    [Google Scholar]
  16. Ferguson A. D., Hofmann E., Coulton J. W., Diederichs K., Welte W.. 1998; Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science282:2215–2220
    [Google Scholar]
  17. Folschweiller N., Schalk I. J., Celia H., Kieffer B., Abdallah M. A., Pattus F.. 2000; The pyoverdin receptor FpvA, a TonB-dependent receptor involved in iron uptake by Pseudomonas aeruginosa . Mol Membr Biol17:123–133
    [Google Scholar]
  18. Gaballa A., Koedam N., Cornelis P.. 1996; Involvement of a cytochrome c biogenesis gene in pyoverdine production in Pseudomonas fluorescens ATCC 17400. Mol Microbiol21:777–785
    [Google Scholar]
  19. Gaballa A., Baysse C., Koedam N., Muyldermans S., Cornelis P.. 1998; Different residues in periplasmic domains of the CcmC inner membrane protein of Pseudomonas fluorescens ATCC 17400 are critical for cytochromes c biogenesis and pyoverdine-mediated iron uptake. Mol Microbiol30:547–555
    [Google Scholar]
  20. Goldman B. S., Kranz R. G.. 2001; ABC transporters associated with cytochrome c biogenesis. Res Microbiol152:323–329
    [Google Scholar]
  21. Govan J. R. W., Deretic V.. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev60:539–574
    [Google Scholar]
  22. Hanahan D.. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580
    [Google Scholar]
  23. Handfield M., Lehoux D. E., Sanschagrin F., Mahan M. J., Woods D. E., Levesque R. C.. 2000; In vivo -induced genes in Pseudomonas aeruginosa . Infect Immun68:2359–2362
    [Google Scholar]
  24. Herrero M., de Lorenzo V., Timmis K. N.. 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]
  25. 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]
  26. Höfte M., Buysens S., Koedam N., Cornelis P.. 1993; Zinc affects siderophore-mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Bio/Metals6:85–91
    [Google Scholar]
  27. Hohnadel D., Meyer J. M.. 1988; Specificity of pyoverdine-mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol170:4865–4873
    [Google Scholar]
  28. Jones A. M., Govan J. R., Doherty C. J., Dodd M. E., Isalska B. J., Stanbridge T. N., Webb A. K.. 2001; Spread of a multiresistant strain of Pseudomonas aeruginosa in an adult cystic fibrosis clinic. Lancet358:557–558
    [Google Scholar]
  29. 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
    [Google Scholar]
  30. 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]
  31. Lamont I. A., Beare P. A., Ochsner U., Vasil A. I., Vasil M. L.. 2002; Siderophore-mediated signaling mediates virulence factor production in Pseudomonas aeruginosa . Proc Natl Acad Sci U S A99:7072–7077
    [Google Scholar]
  32. Lim A. Jr, De Vos D., Brauns M., Mossialos D., Gaballa A., Qing D., Cornelis P.. 1997; Molecular and immunological characterization of OprL, the 18 kDa outer-membrane peptidoglycan-associated lipoprotein (PAL) of Pseudomonas aeruginosa . Microbiology143:1709–1716
    [Google Scholar]
  33. McCallum S. J., Corkill J., Gallagher M., Ledson M. J., Hart C. A., Walshaw M. J.. 2001; Superinfection with a transmissible strain of Pseudomonas aeruginosa in adults with cystic fibrosis chronically colonised by P aeruginosa . Lancet358:558–560
    [Google Scholar]
  34. McCallum S. J., Gallagher M. J., Corkill J. E., Hart C. A., Ledson M. J., Walshaw M. J.. 2002; Spread of an epidemic Pseudomonas aeruginosa strain from a patient with cystic fibrosis (CF) to non-CF relatives. Thorax57:559–560
    [Google Scholar]
  35. McMorran B. J., Merriman M. E., Rombel I. T., Lamont I. L.. 1996; Characterization of the pvdE gene which is required for pyoverdine synthesis in Pseudomonas aeruginosa . Gene176:55–59
    [Google Scholar]
  36. Meyer J. M.. 2000; Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch Microbiol174:135–142
    [Google Scholar]
  37. Meyer J. M., Neely A., Stintzi A., Georges C., Holder I. A.. 1996; Pyoverdin is essential for virulence of Pseudomonas aeruginosa . Infect Immun64:518–523
    [Google Scholar]
  38. 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
    [Google Scholar]
  39. Meyer J. M., Stintzi A., Poole K.. 1999; The ferripyoverdine receptor FpvA of Pseudomonas aeruginosa PAO1 recognizes the ferripyoverdines of P. aeruginosa PAO1 and P. fluorescens ATCC 13525. FEMS Microbiol Lett170:145–150
    [Google Scholar]
  40. Meyer J. M., Geoffroy V., Baysse C., Cornelis P., Barelmann I., Taraz K., Budzikiewicz H.. 2002; Siderophore-mediated iron uptake in fluorescent Pseudomonas : characterization of the pyoverdine-receptor binding site of three cross-reacting pyoverdines. Arch Biochem Biophys397:179–183
    [Google Scholar]
  41. Michel-Briand Y., Baysse C.. 2002; The pyocins of Pseudomonas aeruginosa . Biochimie84:499–510
    [Google Scholar]
  42. Mizuno T., Kageyama M.. 1978; Separation and characterization of the outer membrane of Pseudomonas aeruginosa . J Biochem84:179–191
    [Google Scholar]
  43. 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 Pseudomonas sp. strain M114. Mol Gen Genet242:9–16
    [Google Scholar]
  44. Mossialos D., Meyer J. M., Budzikiewicz H., Wolff U., Koedam N., Baysse C., Anjaiah V., Cornelis P.. 2000; Quinolobactin, a new siderophore of Pseudomonas fluorescens ATCC 17400 whose production is repressed by the cognate pyoverdine. Appl Environ Microbiol66:487–492
    [Google Scholar]
  45. Munsch P., Geoffroy V. A., Alatossava T., Meyer J. M.. 2000; Application of siderotyping for characterization of Pseudomonas tolaasii and ‚ Pseudomonas reactans ' isolates associated with brown blotch disease of cultivated mushrooms. Appl Environ Microbiol66:4834–4841
    [Google Scholar]
  46. Neilands J. B.. 1995; Siderophores: structure and function of microbial iron transport compounds. J Biol Chem270:26723–26726
    [Google Scholar]
  47. Nouwens A. S., Cordwell S. J., Larsen M. R., Molloy M. P., Gillings M., Willcox M. D., Walsh B. J.. 2000; Complementing genomics with proteomics: the membrane subproteome of Pseudomonas aeruginosa PAO1. Electrophoresis21:3797–3809
    [Google Scholar]
  48. Ochsner U. A., Snyder A., Vasil A. I., Vasil M. L.. 2002a; Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci U S A99:8312–8317
    [Google Scholar]
  49. Ochsner U. A., Wilderman P. J., Vasil A. I., Vasil M. L.. 2002b; GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa : identification of novel pyoverdine biosynthesis genes. Mol Microbiol45:1277–1287
    [Google Scholar]
  50. Parsons Y. N., Panagea S., Smart C. H., Walshaw M. J., Hart C. A., Winstanley C.. 2002; Use of subtractive hybridization to identify a diagnostic probe for a cystic fibrosis epidemic strain of Pseudomonas aeruginosa . J Clin Microbiol40:4607–4611
    [Google Scholar]
  51. 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
    [Google Scholar]
  52. Poole K., Neshat S., Krebes K., Heinrichs D. E.. 1993; Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa . J Bacteriol175:4597–4604
    [Google Scholar]
  53. Ratledge C., Dover L. G.. 2000; Iron metabolism in pathogenic bacteria. Annu Rev Microbiol54:881–941
    [Google Scholar]
  54. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  55. Schalk I. J., Hennard C., Dugave C., Poole K., Abdallah M. A., Pattus F.. 2001; Iron-free pyoverdin binds to its outer membrane receptor FpvA in Pseudomonas aeruginosa : a new mechanism for membrane iron transport. Mol Microbiol39:351–360
    [Google Scholar]
  56. Schalk I. J., Abdallah M. A., Pattus F.. 2002; Recycling of pyoverdin on the FpvA receptor after ferric pyoverdin uptake and dissociation in Pseudomonas aeruginosa . Biochemistry41:1663–1671
    [Google Scholar]
  57. Shen J., Meldrum A., Poole K.. 2002; FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa . J Bacteriol184:3268–3275
    [Google Scholar]
  58. Takase H., Nitanai H., Hoshino K., Otani T.. 2000a; Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect Immun68:4498–4504
    [Google Scholar]
  59. Takase H., Nitanai H., Hoshino K., Otani T.. 2000b; Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect Immun68:1834–1839
    [Google Scholar]
  60. Thöny-Meyer L.. 1997; Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev61:337–376
    [Google Scholar]
  61. Van den Eede G., Deblaere R., Goethals K., van Montagu M., Holsters M.. 1992; Broad-host-range and promoter selection vectors for bacteria that interact with plants. Mol Plant–Microbe Interact5:228–234
    [Google Scholar]
  62. Van Haute E., Joos H., Maes M., Warren M., Van Montagu M.. 1983; Intergenic transfer and recombination of restriction fragments cloned in pBR322: a novel strategy for the reversed genetics of the Ti plasmid of Agrobacterium tumefaciens . EMBO J2:411–417
    [Google Scholar]
  63. Visca P., Leoni L., Wilson M. J., Lamont I. L.. 2002; Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas . Mol Microbiol45:1177–1190
    [Google Scholar]
  64. Wilson M. J., McMorran B. J., Lamont I. L.. 2001; Analysis of promoters recognized by PvdS, an extracytoplasmic-function sigma factor protein from Pseudomonas aeruginosa . J Bacteriol183:2151–2155
    [Google Scholar]
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