
f Roles of the TonB1 and TonB2 proteins in haemin iron acquisition and virulence in Riemerella anatipestifer
- Authors: Shuang Miao1 , Linlin Xing1 , Jingjing Qi1 , Hui Yu1 , Pan Jiang1 , Bingqing Sun1 , Junsheng Cui1 , Changcan Ou1 , Qinghai Hu1
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- VIEW AFFILIATIONS
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1 Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, 518 Ziyue Road, Shanghai 200241, PR China
- Correspondence Qinghai Hu [email protected]
- First Published Online: 01 August 2015, Microbiology 161: 1592-1599, doi: 10.1099/mic.0.000123
- Subject: Host-Microbe Interaction
- Received:
- Accepted:
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Roles of the TonB1 and TonB2 proteins in haemin iron acquisition and virulence in Riemerella anatipestifer, Page 1 of 1
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Two TonB systems in Riemerella anatipestifer were found and characterized as ExbB1–ExbD1–TonB1 and ExbB2–ExbD2–ExbD2′–TonB2, but the significance of two sets of TonB complexes in R. anatipestifer is not clear. In this study, by deleting the tonB1 or tonB2 gene of R. anatipestifer 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 l-cysteine, but haemin iron acquisition was defective in the CH3ΔtonB1 mutant, and the deletion of either tonB1 or tonB2 significantly reduced adhesion to and invasion of Vero cells. Animal experiments indicated that the LD50 of the CH3ΔtonB1 and CH3ΔtonB2 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 CH3ΔtonB1 or CH3ΔtonB2 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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The GenBank/EMBL/DDBJ accession numbers for the sequences of the TonB1 and TonB2 systems in Riemerella anatipestifer strain CH3 are KM393215 and KM393216, respectively.
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One supplementary table and two supplementary figures are available with the online Supplementary Material.
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Edited by: D. Nies
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Abbreviation: DIP 2,2′-dipyridyl
© 2015 The Authors
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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 Microbiol 108: 246––255 [CrossRef] [PubMed].
-
Andrews S.C. , Robinson A.K. , Rodríguez-Quiñones F. . ( 2003;). Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215––237 [CrossRef] [PubMed].
-
Banin E. , Vasil M.L. , Greenberg E.P. . ( 2005;). Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102: 11076––11081 [CrossRef] [PubMed].
-
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 Immun 72: 701––708 [CrossRef] [PubMed].
-
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 One 2: e224 [CrossRef] [PubMed].
-
Braun V. , Hantke K. . ( 2011;). Recent insights into iron import by bacteria. Curr Opin Chem Biol 15: 328––334 [CrossRef] [PubMed].
-
Crosa J.H. . ( 1989;). Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev 53: 517––530 [PubMed].
-
Faraldo-Gómez J.D. , Sansom M.S. . ( 2003;). Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4: 105––116 [CrossRef] [PubMed].
-
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 Microbiol 71: 79––91 [CrossRef] [PubMed].
-
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 Med 34: 8––9 (in Chinese).
-
Hu Q. , Han X. , Zhou X. , Ding C. , Zhu Y. , Yu S. . ( 2011;). OmpA is a virulence factor of Riemerella anatipestifer . Vet Microbiol 150: 278––283 [CrossRef] [PubMed].
-
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 Methods 95: 262––267 [CrossRef] [PubMed].
-
Huynh C. , Andrews N.W. . ( 2008;). Iron acquisition within host cells and the pathogenicity of Leishmania . Cell Microbiol 10: 293––300 [CrossRef] [PubMed].
-
Krewulak K.D. , Vogel H.J. . ( 2011;). TonB or not TonB: is that the question?. Biochem Cell Biol 89: 87––97 [CrossRef] [PubMed].
-
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 Microbiol 167: 713––718 [CrossRef] [PubMed].
-
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 Sci 4: 144––153 [PubMed].[CrossRef]
-
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 Microbiol 69: 5907––5913 [CrossRef] [PubMed].
-
Nairz M. , Schroll A. , Sonnweber T. , Weiss G. . ( 2010;). The struggle for iron – a metal at the host–pathogen interface. Cell Microbiol 12: 1691––1702 [CrossRef] [PubMed].
-
Noinaj N. , Guillier M. , Barnard T.J. , Buchanan S.K. . ( 2010;). TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64: 43––60 [CrossRef] [PubMed].
-
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. Science 312: 1399––1402 [CrossRef] [PubMed].
-
Philippe N. , Alcaraz J.P. , Coursange E. , Geiselmann J. , Schneider D. . ( 2004;). Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51: 246––255 [CrossRef] [PubMed].
-
Reed M.J. , Muench H. . ( 1938;). A simple method of estimating fifty percent endpoints. Am J Hyg 27: 493––497.
-
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?. Biometals 20: 365––377 [CrossRef] [PubMed].
-
Sandhu T.S. . ( 2008;). Rimerella anatipestifer infection. . In Diseases of Poultry, pp. 758––764. Edited by Saif Y. S. . , 12th edn. Ames, IA: Blackwell;.
-
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 Microbiol 63: 1054––1068 [CrossRef] [PubMed].
-
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 Microbiol 39: 801––812 [CrossRef] [PubMed].
-
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 Immun 72: 7326––7329 [CrossRef] [PubMed].
-
Tai S.S. , Lee C.J. , Winter R.E. . ( 1993;). Hemin utilization is related to virulence of Streptococcus pneumoniae . Infect Immun 61: 5401––5405 [PubMed].
-
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 Microbiol 168: 395––402 [CrossRef] [PubMed].
-
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 Microbiol 190: 595––603 [CrossRef] [PubMed].
-
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 Genomics 15: 479 [CrossRef] [PubMed].
-
Wyckoff E.E. , Mey A.R. , Payne S.M. . ( 2007;). Iron acquisition in Vibrio cholerae . Biometals 20: 405––416 [CrossRef] [PubMed].
-
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 Bacteriol 193: 2896––2897 [CrossRef] [PubMed].

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