This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Supplemental material
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
Google Scholar
Right arrow Articles by Sikora, A. E.
Right arrow Articles by Sandkvist, M.
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sikora, A. E.
Right arrow Articles by Sandkvist, M.

 Previous Article  |  Next Article 

Journal of Bacteriology, September 2009, p. 5398-5408, Vol. 191, No. 17
0021-9193/09/$08.00+0     doi:10.1128/JB.00092-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Cell Envelope Perturbation Induces Oxidative Stress and Changes in Iron Homeostasis in Vibrio cholerae{triangledown} ,{dagger}

Aleksandra E. Sikora,1 Sinem Beyhan,2 Michael Bagdasarian,3 Fitnat H. Yildiz,2 and Maria Sandkvist1*

Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor,1 Department of Microbiology, Michigan State University, East Lansing, Michigan,3 Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, California2

Received 23 January 2009/ Accepted 14 June 2009

The Vibrio cholerae type II secretion (T2S) machinery is a multiprotein complex that spans the cell envelope. When the T2S system is inactivated, cholera toxin and other exoproteins accumulate in the periplasmic compartment. Additionally, loss of secretion via the T2S system leads to a reduced growth rate, compromised outer membrane integrity, and induction of the extracytoplasmic stress factor RpoE (A. E. Sikora, S. R. Lybarger, and M. Sandkvist, J. Bacteriol. 189:8484-8495, 2007). In this study, gene expression profiling reveals that inactivation of the T2S system alters the expression of genes encoding cell envelope components and proteins involved in central metabolism, chemotaxis, motility, oxidative stress, and iron storage and acquisition. Consistent with the gene expression data, molecular and biochemical analyses indicate that the T2S mutants suffer from internal oxidative stress and increased levels of intracellular ferrous iron. By using a tolA mutant of V. cholerae that shares a similar compromised membrane phenotype but maintains a functional T2S machinery, we show that the formation of radical oxygen species, induction of oxidative stress, and changes in iron physiology are likely general responses to cell envelope damage and are not unique to T2S mutants. Finally, we demonstrate that disruption of the V. cholerae cell envelope by chemical treatment with polymyxin B similarly results in induction of the RpoE-mediated stress response, increased sensitivity to oxidants, and a change in iron metabolism. We propose that many types of extracytoplasmic stresses, caused either by genetic alterations of outer membrane constituents or by chemical or physical damage to the cell envelope, induce common signaling pathways that ultimately lead to internal oxidative stress and misregulation of iron homeostasis.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI. Phone: (734) 764-3552. Fax: (734) 764-3562. E-mail: mariasan{at}umich.edu

{triangledown} Published ahead of print on 19 June 2009.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, September 2009, p. 5398-5408, Vol. 191, No. 17
0021-9193/09/$08.00+0     doi:10.1128/JB.00092-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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