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Journal of Bacteriology, November 2009, p. 6555-6570, Vol. 191, No. 21
0021-9193/09/$08.00+0     doi:10.1128/JB.00949-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

The Vibrio cholerae Flagellar Regulatory Hierarchy Controls Expression of Virulence Factors{triangledown} ,{dagger}

Khalid Ali Syed,1 Sinem Beyhan,2 Nidia Correa,1 Jessica Queen,3 Jirong Liu,1 Fen Peng,1 Karla J. F. Satchell,3 Fitnat Yildiz,2 and Karl E. Klose1*

South Texas Center for Emerging Infectious Diseases and Department of Biology, The University of Texas at San Antonio, San Antonio, Texas,1 Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, Santa Cruz, California,2 Department of Microbiology-Immunology, Northwestern University Medical School, Evanston, Illinois3

Received 20 July 2009/ Accepted 24 August 2009

Vibrio cholerae is a motile bacterium responsible for the disease cholera, and motility has been hypothesized to be inversely regulated with virulence. We examined the transcription profiles of V. cholerae strains containing mutations in flagellar regulatory genes (rpoN, flrA, flrC, and fliA) by utilizing whole-genome microarrays. Results revealed that flagellar transcription is organized into a four-tiered hierarchy. Additionally, genes with proven or putative roles in virulence (e.g., ctx, tcp, hemolysin, and type VI secretion genes) were upregulated in flagellar regulatory mutants, which was confirmed by quantitative reverse transcription-PCR. Flagellar regulatory mutants exhibit increased hemolysis of human erythrocytes, which was due to increased transcription of the thermolabile hemolysin (tlh). The flagellar regulatory system positively regulates transcription of a diguanylate cyclase, CdgD, which in turn regulates transcription of a novel hemagglutinin (frhA) that mediates adherence to chitin and epithelial cells and enhances biofilm formation and intestinal colonization in infant mice. Our results demonstrate that the flagellar regulatory system modulates the expression of nonflagellar genes, with induction of an adhesin that facilitates colonization within the intestine and repression of virulence factors maximally induced following colonization. These results suggest that the flagellar regulatory hierarchy facilitates correct spatiotemporal expression patterns for optimal V. cholerae colonization and disease progression.

* Corresponding author. Mailing address: Dept. of Biology, University of Texas at San Antonio, One UTSA Circle, San Antonio, TX 78249. Phone: (210) 458-6140. Fax: (210) 458-4468. E-mail: Karl.Klose{at}utsa.edu

{triangledown} Published ahead of print on 28 August 2009.

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

Journal of Bacteriology, November 2009, p. 6555-6570, Vol. 191, No. 21
0021-9193/09/$08.00+0     doi:10.1128/JB.00949-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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