1887

Abstract

Two TonB systems in were found and characterized as ExbB1–ExbD1–TonB1 and ExbB2–ExbD2–ExbD2′–TonB2, but the significance of two sets of TonB complexes in is not clear. In this study, by deleting the or gene of strain CH3, we investigated the roles of the TonB1 and TonB2 proteins in iron acquisition and virulence. The results showed that strain CH3 could utilize haemin as the sole iron source in the presence of -cysteine, but haemin iron acquisition was defective in the CH3Δ mutant, and the deletion of either or significantly reduced adhesion to and invasion of Vero cells. Animal experiments indicated that the LD of the CH3Δ and CH3Δ mutants in ducklings was ∼224- and ∼87-fold, respectively, higher than that of the WT CH3 strain. Additional analysis indicated that blood bacterial loading of ducklings infected with CH3Δ or CH3Δ decreased significantly compared with that found for WT CH3-infected ducklings. Thus, our results indicated that the TonB1, but not TonB2 protein, is involved in haemin iron acquisition and that both TonB proteins are necessary for optimal bacterial virulence.

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2015-08-01
2020-04-04
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References

  1. Alves J.R., Pereira A.C.M., Souza M.C., Costa S.B., Pinto A.S., Mattos-Guaraldi A.L., Hirata-Júnior R., Rosa A.C.P., Asad L.M.B.O.. 2010; Iron-limited condition modulates biofilm formation and interaction with human epithelial cells of enteroaggregative Escherichia coli (EAEC). J Appl Microbiol108:246–255 [CrossRef][PubMed]
    [Google Scholar]
  2. Andrews S.C., Robinson A.K., Rodríguez-Quiñones F.. 2003; Bacterial iron homeostasis. FEMS Microbiol Rev27:215–237 [CrossRef][PubMed]
    [Google Scholar]
  3. 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][PubMed]
    [Google Scholar]
  4. Beddek A.J., Sheehan B.J., Bossé J.T., Rycroft A.N., Kroll J.S., Langford P.R.. 2004; Two TonB systems in Actinobacillus pleuropneumoniae: their roles in iron acquisition and virulence. Infect Immun72:701–708 [CrossRef][PubMed]
    [Google Scholar]
  5. Blanvillain S., Meyer D., Boulanger A., Lautier M., Guynet C., Denancé N., Vasse J., Lauber E., Arlat M.. 2007; Plant carbohydrate scavenging through tonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria. PLoS One2:e224 [CrossRef][PubMed]
    [Google Scholar]
  6. Braun V., Hantke K.. 2011; Recent insights into iron import by bacteria. Curr Opin Chem Biol15:328–334 [CrossRef][PubMed]
    [Google Scholar]
  7. Crosa J.H.. 1989; Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev53:517–530[PubMed]
    [Google Scholar]
  8. Faraldo-Gómez J.D., Sansom M.S.. 2003; Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol4:105–116 [CrossRef][PubMed]
    [Google Scholar]
  9. Hagan E.C., Mobley H.L.. 2009; Haem acquisition is facilitated by a novel receptor Hma and required by uropathogenic Escherichia coli for kidney infection. Mol Microbiol71:79–91 [CrossRef][PubMed]
    [Google Scholar]
  10. Hu Q., Chen H., Liu X., Zhan M., Zhang Z., Deen S., Zhang Y.. 2002; [Determination of growth curve of Riemerella anatipestifer]. Animal Husbandry Vet Med34:8–9 (in Chinese)
    [Google Scholar]
  11. Hu Q., Han X., Zhou X., Ding C., Zhu Y., Yu S.. 2011; OmpA is a virulence factor of Riemerella anatipestifer . Vet Microbiol150:278–283 [CrossRef][PubMed]
    [Google Scholar]
  12. Hu Q., Miao S., Ni X., Lu F., Yu H., Xing L., Jiang P.. 2013; Construction of a shuttle vector for use in Riemerella anatipestifer . J Microbiol Methods95:262–267 [CrossRef][PubMed]
    [Google Scholar]
  13. Huynh C., Andrews N.W.. 2008; Iron acquisition within host cells and the pathogenicity of Leishmania . Cell Microbiol10:293–300 [CrossRef][PubMed]
    [Google Scholar]
  14. Krewulak K.D., Vogel H.J.. 2011; TonB or not TonB: is that the question?. Biochem Cell Biol89:87–97 [CrossRef][PubMed]
    [Google Scholar]
  15. Lu F., Miao S., Tu J., Ni X., Xing L., Yu H., Pan L., Hu Q.. 2013; The role of TonB-dependent receptor TbdR1 in Riemerella anatipestifer in iron acquisition and virulence. Vet Microbiol167:713–718 [CrossRef][PubMed]
    [Google Scholar]
  16. Mavromatis K., Lu M., Misra M., Lapidus A., Nolan M., Lucas S., Hammon N., Deshpande S., Cheng J.F., other authors. 2011; Complete genome sequence of Riemerella anatipestifer type strain (ATCC 11845). Stand Genomic Sci4:144–153[PubMed][CrossRef]
    [Google Scholar]
  17. Moreira L.O., Andrade A.F., Vale M.D., Souza S.M., Hirata R. Jr, Asad L.M., Asad N.R., Monteiro-Leal L.H., Previato J.O., Mattos-Guaraldi A.L.. 2003; Effects of iron limitation on adherence and cell surface carbohydrates of Corynebacterium diphtheriae strains. Appl Environ Microbiol69:5907–5913 [CrossRef][PubMed]
    [Google Scholar]
  18. Nairz M., Schroll A., Sonnweber T., Weiss G.. 2010; The struggle for iron – a metal at the host–pathogen interface. Cell Microbiol12:1691–1702 [CrossRef][PubMed]
    [Google Scholar]
  19. 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]
  20. Pawelek P.D., Croteau N., Ng-Thow-Hing C., Khursigara C.M., Moiseeva N., Allaire M., Coulton J.W.. 2006; Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science312:1399–1402 [CrossRef][PubMed]
    [Google Scholar]
  21. Philippe N., Alcaraz J.P., Coursange E., Geiselmann J., Schneider D.. 2004; Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid51:246–255 [CrossRef][PubMed]
    [Google Scholar]
  22. Reed M.J., Muench H.. 1938; A simple method of estimating fifty percent endpoints. Am J Hyg27:493–497
    [Google Scholar]
  23. Rhodes E.R., Menke S., Shoemaker C., Tomaras A.P., McGillivary G., Actis L.A.. 2007; Iron acquisition in the dental pathogen Actinobacillus actinomycetemcomitans: what does it use as a source and how does it get this essential metal?. Biometals20:365–377 [CrossRef][PubMed]
    [Google Scholar]
  24. Sandhu T.S.. 2008; Rimerella anatipestifer infection. In Diseases of Poultry pp.758–764 Edited by Saif Y. S.. , 12th edn. Ames, IA: Blackwell;
    [Google Scholar]
  25. Schauer K., Gouget B., Carrière M., Labigne A., de Reuse H.. 2007; Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol Microbiol63:1054–1068 [CrossRef][PubMed]
    [Google Scholar]
  26. 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]
  27. 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]
  28. Tai S.S., Lee C.J., Winter R.E.. 1993; Hemin utilization is related to virulence of Streptococcus pneumoniae . Infect Immun61:5401–5405[PubMed]
    [Google Scholar]
  29. Tu J., Lu F., Miao S., Ni X., Jiang P., Yu H., Xing L., Yu S., Ding C., Hu Q.. 2014; The siderophore-interacting protein is involved in iron acquisition and virulence of Riemerella anatipestifer strain CH3. Vet Microbiol168:395–402 [CrossRef][PubMed]
    [Google Scholar]
  30. Wang Q., Liu Q., Cao X., Yang M., Zhang Y.. 2008; Characterization of two TonB systems in marine fish pathogen Vibrio alginolyticus: their roles in iron utilization and virulence. Arch Microbiol190:595–603 [CrossRef][PubMed]
    [Google Scholar]
  31. Wang X., Liu W., Zhu D., Yang L., Liu M., Yin S., Wang M., Jia R., Chen S., other authors. 2014; Comparative genomics of Riemerella anatipestifer reveals genetic diversity. BMC Genomics15:479 [CrossRef][PubMed]
    [Google Scholar]
  32. Weinberg E.D.. 1978; Iron and infection. Microbiol Rev42:45–66[PubMed]
    [Google Scholar]
  33. Wyckoff E.E., Mey A.R., Payne S.M.. 2007; Iron acquisition in Vibrio cholerae . Biometals20:405–416 [CrossRef][PubMed]
    [Google Scholar]
  34. Yuan J., Liu W., Sun M., Song S., Cai J., Hu S.. 2011; Complete genome sequence of the pathogenic bacterium Riemerella anatipestifer strain RA-GD. J Bacteriol193:2896–2897 [CrossRef][PubMed]
    [Google Scholar]
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