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Volume 153, Issue 5

Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Free

Abstract

In response to iron starvation, produces the siderophore pyochelin. When secreted to the extracellular environment, pyochelin chelates iron and transports it to the bacterial cytoplasm via its specific outer-membrane receptor FptA and the inner-membrane permease FptX. Exogenously added pyochelin also acts as a signal which induces the expression of the pyochelin biosynthesis and uptake genes by activating PchR, a cytoplasmic regulatory protein of the AraC/XylS family. The importance of ferripyochelin uptake genes in this regulation was evaluated. The and genes were shown to be part of the ferripyochelin transport operon, which is conserved in sp. and . The and genes were found to be dispensable for utilization of pyochelin as an iron source, for signalling and for pyochelin production. By contrast, mutations in and not only interfered with pyochelin utilization, but also affected signalling and diminished siderophore production. It is concluded from this that pyochelin-mediated signalling operates to a large extent via the ferripyochelin transport system.

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Keyword(s): Dha, dihydroaeruginoate
SGM
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2007-05-01
2024-04-18
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References

  1. Andrews S. C., Robinson A. K., Rodríguez-Quiñones F. 2003; Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237 [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 Bacteriol 176:307–319
     [Google Scholar]
  3. Beare P. A., For R. J., Martin L. W., Lamont I. L. 2003; Siderophore-mediated cell signaling in Pseudomonas aeruginosa : divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol Microbiol 47:195–207
     [Google Scholar]
  4. Braun V., Killmann H. 1999; Bacterial solutions to the iron-supply problem. Trends Biochem Sci 24:104–109 [CrossRef]
     [Google Scholar]
  5. Carmi R., Carmeli S., Levy E., Gough F. J. 1994; (+)-( S )-dihydroaeruginoic acid, an inhibitor of Septoria tritici and other phytopathogenic fungi and bacteria, produced by Pseudomonas fluorescens. J Nat Prod 57:1200–1205 [CrossRef]
     [Google Scholar]
  6. Cox C. D. 1980; Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol 142:581–587
     [Google Scholar]
  7. Cox C. D., Adams P. 1985; Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun 48:130–138
     [Google Scholar]
  8. Darling P., Chan M., Cox A. D., Sokol P. A. 1998; Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect Immun 66:874–877
     [Google Scholar]
  9. Dean C. R., Poole K. 1993; Expression of the ferric enterobactin receptor (PfeA) of Pseudomonas aeruginosa : Involvement of a two-component regulatory system. Mol Microbiol 8:1095–1103 [CrossRef]
     [Google Scholar]
  10. Dean C. R., Neshat S., Poole K. 1996; PfeR, an enterobactin-responsive activator of ferric enterobactin receptor gene expression in Pseudomonas aeruginosa. J Bacteriol 178:5361–5369
     [Google Scholar]
  11. Del Sal G., Manfioletti G., Schneider C. 1988; A one-tube plasmid DNA mini-preparation suitable for sequencing. Nucleic Acids Res 16:9878 [CrossRef]
     [Google Scholar]
  12. Escolar L., Perez-Martin J., de Lorenzo V. 1999; Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223–6229
     [Google Scholar]
  13. Farinha M. A., Kropinski A. M. 1990; High efficiency electroporation of Pseudomonas aeruginosa using frozen cell suspensions. FEMS Microbiol Lett 58:221–225
     [Google Scholar]
  14. Gaille C., Kast P., Haas D. 2002; Salicylate biosynthesis in Pseudomonas aeruginosa : purification and characterization of PchB, a novel bifunctional enzyme displaying isochorismate pyruvate-lyase and chorismate mutase activities. J Biol Chem 277:21768–21775 [CrossRef]
     [Google Scholar]
  15. Gaille C., Reimmann C., Haas D. 2003; Isochorismate synthase (PchA), the first and rate-limiting enzyme in salicylate biosynthesis in Pseudomonas aeruginosa. J Biol Chem 278:16893–16898 [CrossRef]
     [Google Scholar]
  16. Guerinot M. L. 1994; Microbial iron transport. Annu Rev Microbiol 48:743–772 [CrossRef]
     [Google Scholar]
  17. Hantke K. 2001; Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172–177 [CrossRef]
     [Google Scholar]
  18. Heinrichs D. E., Poole K. 1993; Cloning and sequence analysis of a gene ( pchR ) encoding an AraC family activator of pyochelin and ferripyochelin receptor synthesis in Pseudomonas aeruginosa. J Bacteriol 175:5882–5889
     [Google Scholar]
  19. Heinrichs D. E., Poole K. 1996; PchR, a regulator of ferripyochelin receptor gene ( fptA ) expression in Pseudomonas aeruginosa , functions both as an activator and as a repressor. J Bacteriol 178:2586–2592
     [Google Scholar]
  20. Hussein S., Hantke K., Braun V. 1981; Citrate-dependent iron transport system in Escherichia coli K-12. Eur J Biochem 117:431–437 [CrossRef]
     [Google Scholar]
  21. Köster W. 1997; Transport of iron(III) hydroxamates across the cytoplasmic membrane of Escherichia coli . In Bioorganic Chemistry, Transition Metals in Biology and their Coordination Chemistry pp 56–68 Edited by Trautwein A. X. Wiley-VCH;
     [Google Scholar]
  22. Köster W. 2001; ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12 . Res Microbiol 152:291–301 [CrossRef]
     [Google Scholar]
  23. Lamont I. L., Beare P. A., Ochsner U., Vasil A. I., Vasil M. L. 2002; Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 99:7072–7077 [CrossRef]
     [Google Scholar]
  24. 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 Bacteriol 178:2299–2313
     [Google Scholar]
  25. Meyer M., Abdallah M. A. 1978; The fluorescent pigment of Pseudomonas fluorescens : biosynthesis, purification and physicochemical properties. J Gen Microbiol 107:319–328 [CrossRef]
     [Google Scholar]
  26. Michel L., Jagdeep S., Nguyen-Ngoc T., Reimmann C., González N. 2005; PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol Microbiol 58:495–509 [CrossRef]
     [Google Scholar]
  27. Moeck G. S., Coulton J. W. 1998; TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol 28:675–681
     [Google Scholar]
  28. 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 Bacteriol 186:2996–3005 [CrossRef]
     [Google Scholar]
  29. Poole K., McKay G. A. 2003; Iron acquisition and its control in Pseudomonas aeruginosa : many roads lead to Rome. Front Biosci 8:d661–d686 [CrossRef]
     [Google Scholar]
  30. Prentki P., Krisch H. M. 1984; In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313 [CrossRef]
     [Google Scholar]
  31. Prince R. W., Cox C. D., Vasil M. L. 1993; Coordinate regulation of siderophore and exotoxin A production: molecular cloning and sequencing of the Pseudomonas aeruginosa fur gene. J Bacteriol 175:2589–2598
     [Google Scholar]
  32. Quadri L. E. N., Keating T. A., Patel H. M., Walsh C. T. 1999; Assembly of the Pseudomonas aeruginosa nonribosomal peptide siderophore pyochelin: in vitro reconstitution of aryl-4,2-bisthiazoline synthetase activity from PchD, PchE, and PchF. Biochemistry 38:14941–14954 [CrossRef]
     [Google Scholar]
  33. Redly G. A., Poole K. 2003; Pyoverdine-mediated regulation of FpvA synthesis in Pseudomonas aeruginosa : involvement of a probable extracytoplasmic-function sigma factor, FpvI. J Bacteriol 185:1261–1265 [CrossRef]
     [Google Scholar]
  34. 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. Microbiology 144:3135–3148 [CrossRef]
     [Google Scholar]
  35. Reimmann C., Patel H. M., Serino L., Barone M., Walsh C. T., Haas D. 2001; Essential PchG-dependent reduction in pyochelin biosynthesis of Pseudomonas aeruginosa. J Bacteriol 183:813–820 [CrossRef]
     [Google Scholar]
  36. Rinehart K. L., Staley A. L., Wilson S. R., Ankenbauer R. G., Cox C. D. 1995; Stereochemical assignment of the pyochelins. J Org Chem 60:2786–2791 [CrossRef]
     [Google Scholar]
  37. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  38. Schnider-Keel U., Seematter A., Maurhofer M., Blumer C., Duffy B., Gigot-Bonnefoy C., Reimmann C., Notz R. other authors Défago G. 2000; Autoinduction of 2,4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J Bacteriol 182:1215–1225 [CrossRef]
     [Google Scholar]
  39. Serino L., Reimmann C., Baur H., Beyeler M., Visca P., Haas D. 1995; Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa. Mol Gen Genet 249:217–228 [CrossRef]
     [Google Scholar]
  40. Serino L., Reimmann C., Visca P., Beyeler M., Della Chiesa V., Haas D. 1997; Biosynthesis of pyochelin and dihydroaeruginoic acid requires the iron-regulated pchDCBA operon in Pseudomonas aeruginosa. J Bacteriol 179:248–257
     [Google Scholar]
  41. Simon R., Priefer U., Pühler A. 1983; A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784–790 [CrossRef]
     [Google Scholar]
  42. Stanisich V. A., Holloway B. W. 1972; A mutant sex factor of Pseudomonas aeruginosa. Genet Res 19:91–108 [CrossRef]
     [Google Scholar]
  43. Vasil M. L., Ochsner U. A. 1999; The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 34:399–413 [CrossRef]
     [Google Scholar]
  44. Vieira J., Messing J. 1991; New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189–194 [CrossRef]
     [Google Scholar]
  45. Visca P., Leoni L., Wilson M. J., Lamont I. L. 2002; Iron transport and regulation, cell signaling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45:1177–1190 [CrossRef]
     [Google Scholar]
  46. Visser M. B., Majumdar S., Hani E., Sokol P. A. 2004; Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections. Infect Immun 72:2850–2857 [CrossRef]
     [Google Scholar]
  47. Voisard C., Bull C. T., Keel C., Laville J., Maurhofer M., Schnider U., Haas D., Défago G. 1994; Biocontrol of root diseases by Pseudomonas fluorescens CHA0: current concepts and experimental approaches. In Molecular Ecology of Rhizosphere Microorganisms pp 67–89 Edited by O'Gara F., Dowling D., Boesten B. Weinheim: VCH;
     [Google Scholar]
  48. Wandersman C., Delepelaire P. 2004; Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647 [CrossRef]
     [Google Scholar]
  49. Watson A., Alm R. A., Mattick J. S. 1996; Construction of improved vectors for protein production in Pseudomonas aeruginosa. Gene 172:163–164 [CrossRef]
     [Google Scholar]
  50. Ye R. W., Haas D., Ka J. O., Krishnapillai V., Zimmermann A., Baird C., Tiedje J. M. 1995; Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. J Bacteriol 177:3606–3609
     [Google Scholar]
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Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa
Microbiology 153, 1508 (2007); https://doi.org/10.1099/mic.0.2006/002915-0
/content/journal/micro/10.1099/mic.0.2006/002915-0
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