1887

Abstract

We determined the ability of to utilize enterobactin (Ent) as a xenosiderophore. Homology searches of the genomic sequence revealed the presence of genes that are homologous to the ferric Ent utilization genes, which consist of the iron-repressible outer-membrane protein genes and , and the ATP-binding cassette transport system operon . Moreover, the and genes, which encode transcriptional regulators, were also found immediately upstream of and , respectively. Growth assays of indicated that both and mutants grew well in the presence of Ent under iron-limiting conditions, whereas both the / double mutant and the mutant barely grew under the same conditions. In addition, growth assays of three isogenic mutants demonstrated that the TonB2 system, and to a lesser extent the TonB1 system, can provide energy for both IrgA and VctA to transport ferric Ent. SDS-PAGE analysis showed that expression of both IrgA and VctA was enhanced by the presence of Ent. Complementation of the and mutants with their respective genes resulted in the increased expression of IrgA and VctA, respectively. Finally, reverse transcriptase-quantitative PCR revealed that transcription of the Ent utilization system genes is iron-regulated, and that transcription of and under iron-limiting conditions is further activated by proteins encoded by and , respectively, together with Ent.

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2012-08-01
2020-01-28
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References

  1. Actis L. A., Fish W., Crosa J. H., Kellerman K., Ellenberger S. R., Hauser F. M., Sanders-Loehr J.. ( 1986;). Characterization of anguibactin, a novel siderophore from Vibrio anguillarum 775(pJM1). J Bacteriol167:57–65[PubMed]
    [Google Scholar]
  2. Anderson M. T., Armstrong S. K.. ( 2004;). The BfeR regulator mediates enterobactin-inducible expression of Bordetella enterobactin utilization genes. J Bacteriol186:7302–7311 [CrossRef][PubMed]
    [Google Scholar]
  3. Andrews S. C., Robinson A. K., Rodríguez-Quiñones F.. ( 2003;). Bacterial iron homeostasis. FEMS Microbiol Rev27:215–237 [CrossRef][PubMed]
    [Google Scholar]
  4. Bagg A., Neilands J. B.. ( 1987;). Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli . Biochemistry26:5471–5477 [CrossRef][PubMed]
    [Google Scholar]
  5. Balado M., Osorio C. R., Lemos M. L.. ( 2008;). Biosynthetic and regulatory elements involved in the production of the siderophore vanchrobactin in Vibrio anguillarum . Microbiology154:1400–1413 [CrossRef][PubMed]
    [Google Scholar]
  6. Balado M., Osorio C. R., Lemos M. L.. ( 2009;). FvtA is the receptor for the siderophore vanchrobactin in Vibrio anguillarum: utility as a route of entry for vanchrobactin analogues. Appl Environ Microbiol75:2775–2783 [CrossRef][PubMed]
    [Google Scholar]
  7. Beall B., Sanden G. N.. ( 1995;). A Bordetella pertussis fepA homologue required for utilization of exogenous ferric enterobactin. Microbiology141:3193–3205 [CrossRef][PubMed]
    [Google Scholar]
  8. Braun V., Hantke K.. ( 1991;). Genetics of bacterial iron transport. Handbook of Microbial Iron Chelates107–138 Winkelmann G.. Boca Raton, FL: CRC Press;
    [Google Scholar]
  9. Brickman T. J., Armstrong S. K.. ( 2009;). Temporal signaling and differential expression of Bordetella iron transport systems: the role of ferrimones and positive regulators. Biometals22:33–41 [CrossRef][PubMed]
    [Google Scholar]
  10. Brown N. L., Stoyanov J. V., Kidd S. P., Hobman J. L.. ( 2003;). The MerR family of transcriptional regulators. FEMS Microbiol Rev27:145–163 [CrossRef][PubMed]
    [Google Scholar]
  11. Carson S. D., Klebba P. E., Newton S. M., Sparling P. F.. ( 1999;). Ferric enterobactin binding and utilization by Neisseria gonorrhoeae . J Bacteriol181:2895–2901[PubMed]
    [Google Scholar]
  12. Chu B. C., Garcia-Herrero A., Johanson T. H., Krewulak K. D., Lau C. K., Peacock R. S., Slavinskaya Z., Vogel H. J.. ( 2010;). Siderophore uptake in bacteria and the battle for iron with the host; a bird’s eye view. Biometals23:601–611 [CrossRef][PubMed]
    [Google Scholar]
  13. Crosa J. H.. ( 1997;). Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria. Microbiol Mol Biol Rev61:319–336[PubMed]
    [Google Scholar]
  14. Dean C. R., Poole K.. ( 1993;). Cloning and characterization of the ferric enterobactin receptor gene (pfeA) of Pseudomonas aeruginosa . J Bacteriol175:317–324[PubMed]
    [Google Scholar]
  15. 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[PubMed]
    [Google Scholar]
  16. Demarre G., Guérout A. M., Matsumoto-Mashimo C., Rowe-Magnus D. A., Marlière P., Mazel D.. ( 2005;). A new family of mobilizable suicide plasmids based on broad host range R388 plasmid (IncW) and RP4 plasmid (IncPα) conjugative machineries and their cognate Escherichia coli host strains. Res Microbiol156:245–255 [CrossRef][PubMed]
    [Google Scholar]
  17. Escolar L., Pérez-Martín J., de Lorenzo V.. ( 1999;). Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol181:6223–6229[PubMed]
    [Google Scholar]
  18. Fetherston J. D., Bearden S. W., Perry R. D.. ( 1996;). YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol Microbiol22:315–325 [CrossRef][PubMed]
    [Google Scholar]
  19. Funahashi T., Tanabe T., Aso H., Nakao H., Fujii Y., Okamoto K., Narimatsu S., Yamamoto S.. ( 2003;). An iron-regulated gene required for utilization of aerobactin as an exogenous siderophore in Vibrio parahaemolyticus . Microbiology149:1217–1225 [CrossRef][PubMed]
    [Google Scholar]
  20. Funahashi T., Tanabe T., Shiuchi K., Nakao H., Yamamoto S.. ( 2009;). Identification and characterization of genes required for utilization of desferri-ferrichrome and aerobactin in Vibrio parahaemolyticus . Biol Pharm Bull32:359–365 [CrossRef][PubMed]
    [Google Scholar]
  21. Gallegos M. T., Schleif R., Bairoch A., Hofmann K., Ramos J. L.. ( 1997;). Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev61:393–410[PubMed]
    [Google Scholar]
  22. Ghysels B., Ochsner U., Möllman 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][PubMed]
    [Google Scholar]
  23. Goldberg M. B., Boyko S. A., Calderwood S. B.. ( 1991;). Positive transcriptional regulation of an iron-regulated virulence gene in Vibrio cholerae . Proc Natl Acad Sci U S A88:1125–1129 [CrossRef][PubMed]
    [Google Scholar]
  24. Griffiths G. L., Sigel S. P., Payne S. M., Neilands J. B.. ( 1984;). Vibriobactin, a siderophore from Vibrio cholerae . J Biol Chem259:383–385[PubMed]
    [Google Scholar]
  25. Heckman K. L., Pease L. R.. ( 2007;). Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc2:924–932 [CrossRef][PubMed]
    [Google Scholar]
  26. 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 Bacteriol175:5882–5889[PubMed]
    [Google Scholar]
  27. Hollander A., Mercante A. D., Shafer W. M., Cornelissen C. N.. ( 2011;). The iron-repressed, AraC-like regulator MpeR activates expression of fetA in Neisseria gonorrhoeae . Infect Immun79:4764–4776 [CrossRef][PubMed]
    [Google Scholar]
  28. Keen N. T., Tamaki S., Kobayashi D., Trollinger D.. ( 1988;). Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene70:191–197 [CrossRef][PubMed]
    [Google Scholar]
  29. Kuehl C. J., Crosa J. H.. ( 2010;). The TonB energy transduction systems in Vibrio species. Future Microbiol5:1403–1412 [CrossRef][PubMed]
    [Google Scholar]
  30. Kuroda T., Mizushima T., Tsuchiya T.. ( 2005;). Physiological roles of three Na+/H+ antiporters in the halophilic bacterium Vibrio parahaemolyticus . Microbiol Immunol49:711–719[PubMed][CrossRef]
    [Google Scholar]
  31. Maddocks S. E., Oyston P. C.. ( 2008;). Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology154:3609–3623 [CrossRef][PubMed]
    [Google Scholar]
  32. Makino K., Oshima K., Kurokawa K., Yokoyama K., Uda T., Tagomori K., Iijima Y., Najima M., Nakano M.. & other authors ( 2003;). Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae . Lancet361:743–749 [CrossRef][PubMed]
    [Google Scholar]
  33. Mey A. R., Payne S. M.. ( 2003;). Analysis of residues determining specificity of Vibrio cholerae TonB1 for its receptors. J Bacteriol185:1195–1207 [CrossRef][PubMed]
    [Google Scholar]
  34. Mey A. R., Wyckoff E. E., Oglesby A. G., Rab E., Taylor R. K., Payne S. M.. ( 2002;). Identification of the Vibrio cholerae enterobactin receptors VctA and IrgA: IrgA is not required for virulence. Infect Immun70:3419–3426 [CrossRef][PubMed]
    [Google Scholar]
  35. Miethke M., Marahiel M. A.. ( 2007;). Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev71:413–451 [CrossRef][PubMed]
    [Google Scholar]
  36. Moeck G. S., Coulton J. W.. ( 1998;). TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol28:675–681 [CrossRef][PubMed]
    [Google Scholar]
  37. Naka H., Crosa J. H.. ( 2012;). Identification and characterization of a novel outer membrane protein receptor FetA for ferric enterobactin transport in Vibrio anguillarum 775 (pJM1). Biometals25:125–133 [CrossRef][PubMed]
    [Google Scholar]
  38. Noinaj N., Guillier M., Barnard T. J., Buchanan S. K.. ( 2010;). TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol64:43–60 [CrossRef][PubMed]
    [Google Scholar]
  39. Palyada K., Threadgill D., Stintzi A.. ( 2004;). Iron acquisition and regulation in Campylobacter jejuni . J Bacteriol186:4714–4729 [CrossRef][PubMed]
    [Google Scholar]
  40. Peacock R. S., Weljie A. M., Howard S. P., Price F. D., Vogel H. J.. ( 2005;). The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J Mol Biol345:1185–1197 [CrossRef][PubMed]
    [Google Scholar]
  41. 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]
  42. Seliger S. S., Mey A. R., Valle A. M., Payne S. M.. ( 2001;). The two TonB systems of Vibrio cholerae: redundant and specific functions. Mol Microbiol39:801–812 [CrossRef][PubMed]
    [Google Scholar]
  43. Stork M., Di Lorenzo M., Mouriño S., Osorio C. R., Lemos M. L., Crosa J. H.. ( 2004;). Two tonB systems function in iron transport in Vibrio anguillarum, but only one is essential for virulence. Infect Immun72:7326–7329 [CrossRef][PubMed]
    [Google Scholar]
  44. Struyvé M., Moons M., Tommassen J.. ( 1991;). Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol218:141–148 [CrossRef][PubMed]
    [Google Scholar]
  45. Tanabe T., Funahashi T., Nakao H., Miyoshi S., Shinoda S., Yamamoto S.. ( 2003;). Identification and characterization of genes required for biosynthesis and transport of the siderophore vibrioferrin in Vibrio parahaemolyticus . J Bacteriol185:6938–6949 [CrossRef][PubMed]
    [Google Scholar]
  46. Tanabe T., Takata N., Naka A., Moon Y. H., Nakao H., Inoue Y., Narimatsu S., Yamamoto S.. ( 2005;). Identification of an AraC-like regulator gene required for induction of the 78-kDa ferrioxamine B receptor in Vibrio vulnificus . FEMS Microbiol Lett249:309–314 [CrossRef][PubMed]
    [Google Scholar]
  47. Tanabe T., Funahashi T., Okajima N., Nakao H., Takeuchi Y., Miyamoto K., Tsujibo H., Yamamoto S.. ( 2011;). The Vibrio parahaemolyticus pvuA1 gene (formerly termed psuA) encodes a second ferric vibrioferrin receptor that requires tonB2 . FEMS Microbiol Lett324:73–79 [CrossRef][PubMed]
    [Google Scholar]
  48. Vasil M. L., Ochsner U. A.. ( 1999;). The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol34:399–413 [CrossRef][PubMed]
    [Google Scholar]
  49. 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 [CrossRef][PubMed]
    [Google Scholar]
  50. Watnick P. I., Butterton J. R., Calderwood S. B.. ( 1998;). The interaction of the Vibrio cholerae transcription factors, Fur and IrgB, with the overlapping promoters of two virulence genes, irgA and irgB . Gene209:65–70 [CrossRef][PubMed]
    [Google Scholar]
  51. Wyckoff E. E., Mey A. R., Payne S. M.. ( 2007;). Iron acquisition in Vibrio cholerae . Biometals20:405–416 [CrossRef][PubMed]
    [Google Scholar]
  52. Xu F., Zeng X., Haigh R. D., Ketley J. M., Lin J.. ( 2010;). Identification and characterization of a new ferric enterobactin receptor, CfrB, in Campylobacter . J Bacteriol192:4425–4435 [CrossRef][PubMed]
    [Google Scholar]
  53. Yamamoto S., Okujo N., Yoshida T., Matsuura S., Shinoda S.. ( 1994;). Structure and iron transport activity of vibrioferrin, a new siderophore of Vibrio parahaemolyticus . J Biochem115:868–874[PubMed]
    [Google Scholar]
  54. Yamamoto S., Akiyama T., Okujo N., Matsu-ura S., Shinoda S.. ( 1995;). Demonstration of a ferric vibrioferrin-binding protein in the outer membrane of Vibrio parahaemolyticus . Microbiol Immunol39:759–766[PubMed][CrossRef]
    [Google Scholar]
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