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Journal of Bacteriology, August 2004, p. 4864-4874, Vol. 186, No. 15
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.15.4864-4874.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

The Sodium-Driven Flagellar Motor Controls Exopolysaccharide Expression in Vibrio cholerae

Crystal M. Lauriano, Chandradipa Ghosh, Nidia E. Correa, and Karl E. Klose*

Department of Microbiology and Immunology, University of Texas Health Science Center, San Antonio, Texas 78229-3900

Received 8 March 2004/ Accepted 26 March 2004

Vibrio cholerae causes the life-threatening diarrheal disease cholera. This organism persists in aquatic environments in areas of endemicity, and it is believed that the ability of the bacteria to form biofilms in the environment contributes to their persistence. Expression of an exopolysaccharide (EPS), encoded by two vps gene clusters, is essential for biofilm formation and causes a rugose colonial phenotype. We previously reported that the lack of a flagellum induces V. cholerae EPS expression. To uncover the signaling pathway that links the lack of a flagellum to EPS expression, we introduced into a rugose flaA strain second-site mutations that would cause reversion back to the smooth phenotype. Interestingly, mutation of the genes encoding the sodium-driven motor (mot) in a nonflagellated strain reduces EPS expression, biofilm formation, and vps gene transcription, as does the addition of phenamil, which specifically inhibits the sodium-driven motor. Mutation of vpsR, which encodes a response regulator, also reduces EPS expression, biofilm formation, and vps gene transcription in nonflagellated cells. Complementation of a vpsR strain with a constitutive vpsR allele likely to mimic the phosphorylated state (D59E) restores EPS expression and biofilm formation, while complementation with an allele predicted to remain unphosphorylated (D59A) does not. Our results demonstrate the involvement of the sodium-driven motor and suggest the involvement of phospho-VpsR in the signaling cascade that induces EPS expression. A nonflagellated strain expressing EPS is defective for intestinal colonization in the suckling mouse model of cholera and expresses reduced amounts of cholera toxin and toxin-coregulated pili in vitro. Wild-type levels of virulence factor expression and colonization could be restored by a second mutation within the vps gene cluster that eliminated EPS biosynthesis. These results demonstrate a complex relationship between the flagellum-dependent EPS signaling cascade and virulence.

* Corresponding author. Mailing address: Dept. of Biology, Univ. of Texas San Antonio, 6900 N. Loop 1604 West, San Antonio, TX 78249-0662. Phone: (210) 458-6140. Fax: (210) 458-5658. E-mail: kklose{at}utsa.edu.

Journal of Bacteriology, August 2004, p. 4864-4874, Vol. 186, No. 15
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.15.4864-4874.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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