1887

Abstract

utilizes several xenosiderophores under conditions of iron limitation, including the citrate hydroxamate siderophore aerobactin. Analysis of the genome sequence revealed the presence of two genes, (PA4675) and PA1365, encoding proteins displaying significant similarity to the aerobactin outer-membrane receptor, IutA, of . The and PA1365 genes were mutated by insertional inactivation and it was demonstrated that ChtA is the outer-membrane receptor for aerobactin. ChtA also mediated the utilization of rhizobactin 1021 and schizokinen, which are structurally similar to aerobactin. In contrast to the utilization of other xenosiderophores by , there was no apparent redundancy in the utilization of aerobactin, rhizobactin 1021 and schizokinen. The utilization of citrate hydroxamate siderophores by was demonstrated to be TonB1 dependent. A Fur box was identified in the region directly upstream of and it was demonstrated by the Fur titration assay that this region is capable of binding Fur and accordingly that expression of is iron regulated. The PA1365 mutant was unaffected in the utilization of citrate hydroxamate siderophores.

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2006-04-01
2020-10-01
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References

  1. 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[CrossRef]
    [Google Scholar]
  2. Ankenbauer R. G, Quan H. N. 1994; FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa : a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J Bacteriol176:307–319
    [Google Scholar]
  3. Ankenbauer R. G, Sryiosachati S, Cox C. D. 1985; Effects of siderophores on the growth of Pseudomonas aeruginosa in human serum and transferrin. Infect Immun49:132–140
    [Google Scholar]
  4. Ankenbauer R. G, Hanne F, Cox C. D. 1986; Mapping of mutations in Pseudomonas aeruginosa defective in pyoverdin production. J Bacteriol167:7–11
    [Google Scholar]
  5. Banin E, Vasil M. L, Greenberg E. P. 2005; Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A102:11076–11081[CrossRef]
    [Google Scholar]
  6. Beare P. A, For R. J, Martin L. W, 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]
  7. Beringer J. E. 1974; R factor transfer in Rhizobium leguminosarum . J Gen Microbiol84:188–198[CrossRef]
    [Google Scholar]
  8. Birnboim H, Doly J. 1979; A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res7:1513–1523[CrossRef]
    [Google Scholar]
  9. Bitter W, Marugg J. D, de Weger L. A, Tommassen J, Weisbeek P. J. 1991; The ferric-pseudobactin receptor PupA of Pseudomonas putida WCS358: homology to TonB dependent Escherichia coli receptors and specificity of the protein. Mol Microbiol5:647–655[CrossRef]
    [Google Scholar]
  10. Buyer J. S, de Lorenzo V, Neilands J. B. 1991; Production of the siderophore aerobactin by a halophilic pseudomonad. Appl Environ Microbiol57:2246–2250
    [Google Scholar]
  11. Casadaban M. J. 1976; Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol104:521–555
    [Google Scholar]
  12. Chen W. P, Kuo T. T. 1993; A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic Acids Res21:2260[CrossRef]
    [Google Scholar]
  13. 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]
  14. Corpet F. 1988; Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res16:10881–10890[CrossRef]
    [Google Scholar]
  15. Cox C. D. 1980; Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa . J Bacteriol142:581–587
    [Google Scholar]
  16. Cox C. D, Adams P. 1985; Siderophore activity of pyoverdine for Pseudomonas aeruginosa . Infect Immun48:130–138
    [Google Scholar]
  17. Crosa J. H. 1997; Signal transduction and transcriptional and posttranscriptional control or iron regulated genes in bacteria. Microbiol Mol Biol Rev61:319–336
    [Google Scholar]
  18. Cunliffe H. E, Merriman T. R, Lamont I. L. 1995; Cloning and characterization of pvdS , a gene required for pyoverdine synthesis in Pseudomonas aeruginosa : PvdS is probably an alternate sigma factor. J Bacteriol177:2744–2750
    [Google Scholar]
  19. Dean C. R, Neshat S, Poole K. 1996; PfeR, an enterobactin-responsive activator of ferric enterobactin receptor gene expression in Pseudomonas aeruginosa . J Bacteriol178:5361–5369
    [Google Scholar]
  20. Finan T. M, Kunkel B, De Vos G. F, Signer E. R. 1986; Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol167:66–72
    [Google Scholar]
  21. Genco C. A, Dixon D. W. 2001; Emerging strategies in microbial haem capture. Mol Microbiol39:1–11[CrossRef]
    [Google Scholar]
  22. Ghysels B, Dieu B. T, Beatson S. A, Pirnay J. P, Ochsner U. A, Vasil M. L, Cornelis P. 2004; FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa . Microbiology150:1671–1680[CrossRef]
    [Google Scholar]
  23. Ghysels B, Ochsner U, Mollman U, Heinisch L, Vasil M, Cornelis P, Matthijs S. 2005; The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol Lett246:167–174[CrossRef]
    [Google Scholar]
  24. Gilis A, Khan M. A, Cornelis P, Meyer J. M, Mergeay M, van der Lelie D. 1996; Siderophore-mediated iron uptake in Alcaligenes eutrophus CH43 and identification of aleB encoding the ferric iron-alcaligin E receptor. J Bacteriol178:5499–5507
    [Google Scholar]
  25. Gross R. F, Engelbrecht F, Braun V. 1984; Genetic and biochemical characterisation of the aerobactin synthesis operon on pColV. Mol Gen Genet196:74–80[CrossRef]
    [Google Scholar]
  26. Gross R, Engelbrecht F, Braun V. 1985; Identification of the genes and their polypeptide products responsible for aerobactin synthesis by pColV plasmids. Mol Gen Genet201:204–212[CrossRef]
    [Google Scholar]
  27. Hantke K. 1984; Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12. Mol Gen Genet197:337–341[CrossRef]
    [Google Scholar]
  28. Hantke K. 2001; Iron and metal regulation in bacteria. Curr Opin Microbiol4:172–177[CrossRef]
    [Google Scholar]
  29. Heinrichs D. E, Poole K. 1996; PchR, a regulator of ferric pyochelin receptor gene (fptA) expression in Pseudomonas aeruginosa , functions both as an activator and as a repressor. J Bacteriol178:2586–2592
    [Google Scholar]
  30. Heinrichs J. H, Gatlin L. E, Kunsch C, Choi G. H, Hanson M. S. 1999; Identification and characterization of SirA, an iron-regulated protein from Staphylococcus aureus . J Bacteriol181:1436–1443
    [Google Scholar]
  31. Huang B, Ru K, Yuan Z, Whitchurch C. B, Mattick J. S. 2004; tonB3 is required for normal twitching motility and extracellular assembly of type IV pili. J Bacteriol186:4387–4389[CrossRef]
    [Google Scholar]
  32. Inoue H, Nojima H, Okayama H. 1990; High efficiency transformation of Escherichia coli with plasmids. Gene96:23–28[CrossRef]
    [Google Scholar]
  33. Klebba P. E, McIntosh M. A, Neilands J. B. 1982; Kinetics of biosynthesis of iron-regulated membrane proteins in Escherichia coli . J Bacteriol149:880–888
    [Google Scholar]
  34. Köster W. 2001; ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B[sub]12[/sub]. Res Microbiol152:291–301[CrossRef]
    [Google Scholar]
  35. Kovach M. E, Elzer P. H, Hill D. S, Robertson G. T, Farris M. A, Roop R. M, Peterson K. M II. 1995; Four new derivatives of the broad-host range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene166:175–176[CrossRef]
    [Google Scholar]
  36. Leoni L, Ciervo A, Orsi N, Visca P. 1996; Iron-regulated transcription of the pvdA gene in Pseudomonas aeruginosa : effect of Fur and PvdS on promoter activity. J Bacteriol178:2299–2313
    [Google Scholar]
  37. Letain T. E, Postle K. 1997; TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in gram-negative bacteria. Mol Microbiol24:271–283[CrossRef]
    [Google Scholar]
  38. Little P. F. R. 1987; Choice and use of cosmid vectors. In DNA Cloning vol. III pp 33–34 Edited by Glover D. M.. Washington, DC: IRL Press;
    [Google Scholar]
  39. Litwin C. M, Calderwood S. B. 1993; Role of iron in regulation of virulence genes. Clin Microbiol Rev6:137–149
    [Google Scholar]
  40. Liu P. V, Shokrani F. 1978; Biological activities of pyochelins: iron chelating agents of Pseudomonas aeruginosa . Infect Immun22:878–890
    [Google Scholar]
  41. Loper J. A, Henkels M. D. 1999; Utilisation of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere. Appl Environ Microbiol65:5357–5363
    [Google Scholar]
  42. Lynch D, O'Brien J, Welch T, Clarke P, Ó Cuív P, Crosa H.J., O'Connell M. 2001; Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti . J Bacteriol183:2576–2585[CrossRef]
    [Google Scholar]
  43. Meyer J. M. 1992; Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa : possible involvement of porin OprF in iron translocation. J Gen Microbiol138:951–958[CrossRef]
    [Google Scholar]
  44. Michel L, González N, Jagdeep S, Nguyen-Ngoc T, Reimmann C. 2005; PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol Microbiol58:495–509[CrossRef]
    [Google Scholar]
  45. Miller W. G, Leveau J. H, Lindow S. E. 2000; Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact13:1243–1250[CrossRef]
    [Google Scholar]
  46. Miyazaki H, Kato H, Nakazawa T, Tsuda M. 1995; A positive regulatory gene, pvdS , for expression of pyoverdin biosynthetic genes in Pseudomonas aeruginosa PAO. Mol Gen Genet248:17–24[CrossRef]
    [Google Scholar]
  47. Nakai K, Kanehisa M. 1991; Expert system for predicting protein localization sites in Gram-negative bacteria. Proteins11:95–110[CrossRef]
    [Google Scholar]
  48. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. 1997; Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng10:1–6[CrossRef]
    [Google Scholar]
  49. Ó Cuív P, Clarke P, Lynch D, O'Connell M. 2004; Identification of rhtX and fptX , novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa , respectively. J Bacteriol186:2996–3005[CrossRef]
    [Google Scholar]
  50. 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]
  51. Ochsner U. A, Johnson Z, Vasil M. L. 2000; Genetics and regulation of two distinct haem-uptake systems, phu and has , in Pseudomonas aeruginosa . Microbiology146:185–198
    [Google Scholar]
  52. Ochsner U. A, Wilderman P. J, Vasil A. I, Vasil M. A. 2002; GeneChip[sup]®[/sup] expression analysis of the iron starvation response in Pseudomonas aeruginosa : identification of novel pyoverdine biosynthesis genes. Mol Microbiol45:1277–1287[CrossRef]
    [Google Scholar]
  53. O'Connell M, Hynes M. F, Puehler A. 1987; Incompatibility between a Rhizobium Sym plasmid and a Ri plasmid of Agrobacterium . Plasmid18:156–163[CrossRef]
    [Google Scholar]
  54. Palma M, Worgall S, Quadri L. E. 2003; Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch Microbiol180:374–379[CrossRef]
    [Google Scholar]
  55. Payne S. M. 1993; Iron acquisition in microbial pathogenesis. Trends Microbiol1:66–69[CrossRef]
    [Google Scholar]
  56. Poole K, McKay G. A. 2003; Iron acquisition and its control in Pseudomonas aeruginosa : many roads lead to Rome. Front Biosci8:661–686[CrossRef]
    [Google Scholar]
  57. Poole K, Young L, Neshat S. 1990; Enterobactin mediated iron transport in Pseudomonas aeruginosa . J Bacteriol172:6991–6996
    [Google Scholar]
  58. Poole K, Zhao Q, Neshat S, Heinrichs D. E, Dean C. R. 1996; The Pseudomonas aeruginosa tonB gene encodes a novel TonB protein. Microbiology142:1449–1458[CrossRef]
    [Google Scholar]
  59. Prince R. W, Cox C. D, Vasil M. L. 1993; Coordinate regulation of siderophore and exotoxin A expression: molecular cloning and sequencing of the Pseudomonas aeruginosa fur gene. J Bacteriol177:2589–2598
    [Google Scholar]
  60. Quandt J, Hynes M. F. 1993; Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene127:15–21[CrossRef]
    [Google Scholar]
  61. Ratledge C, Dover L. G. 2000; Iron metabolism in pathogenic bacteria. Annu Rev Microbiol54:881–941[CrossRef]
    [Google Scholar]
  62. Rédly G. A, Poole K. 2003; Pyoverdine-mediated regulation of FpvA synthesis in Pseudomonas aeruginosa : involvement of a probable extracytoplasmic-function sigma factor, FpvI. J Bacteriol185:1261–1265[CrossRef]
    [Google Scholar]
  63. Reimmann C, Serino L, Beyeler M, Haas D. 1998; Dihydroaeruginoic acid synthetase and pyochelin synthetase, products of the pchEF genes, are induced by extracellular pyochelin in Pseudomonas aeruginosa . Microbiology144:3135–3148[CrossRef]
    [Google Scholar]
  64. 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]
  65. Stojiljkovic I, Baumler A. J, Hantke K. 1994; Fur regulon in gram-negative bacteria. Identification and characterization of new Escherichia coli iron-regulated genes by a Fur titration assay. J Mol Biol236:531–545[CrossRef]
    [Google Scholar]
  66. Stover C. K, Pham X. Q, Erwin A. L. 28 other authors 2000; Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature406:959–964[CrossRef]
    [Google Scholar]
  67. Takase H, Nitanai H, Hoshino K, Otani T. 2000; Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect Immun68:4498–4504[CrossRef]
    [Google Scholar]
  68. Wilderman P. J, Vasil A. I, Johnson Z, Wilson M. J, Cunliffe H. E, Lamont I. L, Vasil M. L. 2001; Characterization of an endoprotease (PrpL) encoded by a PvdS-regulated gene in Pseudomonas aeruginosa . Infect Immun69:5385–5394[CrossRef]
    [Google Scholar]
  69. Wooldridge K. G, Morrissey J. A, Williams P. H. 1992; Transport of ferric-aerobactin into the periplasm and cytoplasm of Escherichia coli K12: role of envelope-associated proteins and effect of endogenous siderophores. J Gen Microbiol138:597–603[CrossRef]
    [Google Scholar]
  70. Zhao Q, Poole K. 2000; A second tonB gene in Pseudomonas aeruginosa is linked to the exbB and exbD genes. Microbiology184:127–132
    [Google Scholar]
  71. Zhao Q, Poole K. 2002; Mutational analysis of the TonB1 energy coupler of Pseudomonas aeruginosa . J Bacteriol184:1503–1513[CrossRef]
    [Google Scholar]
  72. Zhao Q, Li X.-Z, Mistry A, Srikumar R, Zhang L, Lomovskaya O, Poole K. 1998; Influence of the TonB energy-coupling protein on efflux-mediated multidrug resistance in Pseudomonas aeruginosa . Antimicrob Agents Chemother42:2225–2231
    [Google Scholar]
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