This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Reeves, S. A.
Right arrow Articles by Payne, S. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Reeves, S. A.
Right arrow Articles by Payne, S. M.

 Previous Article  |  Next Article 

Infection and Immunity, November 2000, p. 6329-6336, Vol. 68, No. 11
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

TonB Is Required for Intracellular Growth and Virulence of Shigella dysenteriae

Stephanie A. Reeves, Alfredo G. Torres,dagger and Shelley M. Payne*

Section of Molecular Genetics and Microbiology and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712

Received 13 July 2000/Returned for modification 14 August 2000/Accepted 21 August 2000

To assess the importance of TonB-dependent iron transport systems to growth of Shigella in vivo, a tonB mutant of Shigella dysenteriae was isolated and tested in cultured cells. The tonB mutant invaded epithelial cells, but did not form plaques in confluent monolayers of Henle cells, indicating an inability of this mutant to spread from cell to cell. The rate of intracellular multiplication of the tonB mutant was reduced significantly compared to that of the wild type. The loss of virulence in the tonB mutant was not due to loss of either Shu or Ent, the TonB-dependent systems which allow for transport of heme and ferrienterobactin, respectively. A shuA mutant lacking the outer membrane receptor for heme, an entB mutant defective in enterobactin synthesis, and a shuA entB double mutant each were able to invade cultured cells, multiply intracellularly, and form wild-type plaques. The ability of S. dysenteriae to access iron during intracellular growth was assessed by flow cytometric analysis of an iron- and Fur-regulated shuA-gfp reporter construct. Low levels of green fluorescent protein expression in the intracellular environment were observed in all strains, indicating that iron is available to intracellular bacteria, even in the absence of TonB-dependent iron transport. The failure of the tonB mutant to grow well in an iron-replete intracellular environment suggests that TonB plays a role in addition to heme- and siderophore-mediated iron acquisition in vivo, and this function is required for the intracellular growth and intercellular spread of S. dysenteriae.

* Corresponding author. Mailing address: Section of Molecular Genetics and Microbiology, University of Texas, Austin, TX 78712-1095. Phone: (512) 471-9258. Fax: (512) 471-7088. E-mail: payne{at}mail.utexas.edu.

dagger Present address: Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, MD 21201.

Infection and Immunity, November 2000, p. 6329-6336, Vol. 68, No. 11
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Alvarez, B., Alvarez, J., Menendez, A., Guijarro, J. A. (2008). A mutant in one of two exbD loci of a TonB system in Flavobacterium psychrophilum shows attenuated virulence and confers protection against cold water disease. Microbiology 154: 1144-1151 [Abstract] [Full Text]  
  • Paulley, J. T., Anderson, E. S., Roop, R. M. II (2007). Brucella abortus Requires the Heme Transporter BhuA for Maintenance of Chronic Infection in BALB/c Mice. Infect. Immun. 75: 5248-5254 [Abstract] [Full Text]  
  • Sebaihia, M., Preston, A., Maskell, D. J., Kuzmiak, H., Connell, T. D., King, N. D., Orndorff, P. E., Miyamoto, D. M., Thomson, N. R., Harris, D., Goble, A., Lord, A., Murphy, L., Quail, M. A., Rutter, S., Squares, R., Squares, S., Woodward, J., Parkhill, J., Temple, L. M. (2006). Comparison of the Genome Sequence of the Poultry Pathogen Bordetella avium with Those of B. bronchiseptica, B. pertussis, and B. parapertussis Reveals Extensive Diversity in Surface Structures Associated with Host Interaction.. J. Bacteriol. 188: 6002-6015 [Abstract] [Full Text]  
  • Torres, A. G., Jeter, C., Langley, W., Matthysse, A. G. (2005). Differential Binding of Escherichia coli O157:H7 to Alfalfa, Human Epithelial Cells, and Plastic Is Mediated by a Variety of Surface Structures. Appl. Environ. Microbiol. 71: 8008-8015 [Abstract] [Full Text]  
  • Lucchini, S., Liu, H., Jin, Q., Hinton, J. C. D., Yu, J. (2005). Transcriptional Adaptation of Shigella flexneri during Infection of Macrophages and Epithelial Cells: Insights into the Strategies of a Cytosolic Bacterial Pathogen. Infect. Immun. 73: 88-102 [Abstract] [Full Text]  
  • Stork, M., Di Lorenzo, M., Mourino, 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 [Abstract] [Full Text]  
  • Danese, I., Haine, V., Delrue, R.-M., Tibor, A., Lestrate, P., Stevaux, O., Mertens, P., Paquet, J.-Y., Godfroid, J., De Bolle, X., Letesson, J.-J. (2004). The Ton System, an ABC Transporter, and a Universally Conserved GTPase Are Involved in Iron Utilization by Brucella melitensis 16M. Infect. Immun. 72: 5783-5790 [Abstract] [Full Text]  
  • Beddek, A. J., Sheehan, B. J., Bosse, 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 [Abstract] [Full Text]  
  • Runyen-Janecky, L. J., Reeves, S. A., Gonzales, E. G., Payne, S. M. (2003). Contribution of the Shigella flexneri Sit, Iuc, and Feo Iron Acquisition Systems to Iron Acquisition In Vitro and in Cultured Cells. Infect. Immun. 71: 1919-1928 [Abstract] [Full Text]  
  • Runyen-Janecky, L. J., Payne, S. M. (2002). Identification of Chromosomal Shigella flexneri Genes Induced by the Eukaryotic Intracellular Environment. Infect. Immun. 70: 4379-4388 [Abstract] [Full Text]  
  • Torres, A. G., Redford, P., Welch, R. A., Payne, S. M. (2001). TonB-Dependent Systems of Uropathogenic Escherichia coli: Aerobactin and Heme Transport and TonB Are Required for Virulence in the Mouse. Infect. Immun. 69: 6179-6185 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»