Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae

Journal of Bacteriology

Volumn 193, Issue 22, 2011, Pages 6331-6341

  Srivastava, Disha ^a   Harris, Rebecca C ^a   Waters, Christopher M ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOIN; BACTERIAL PROTEIN; CYCLIC DIGMP; CYCLIC GMP; PROTEIN APHA; PROTEIN VPSR; PROTEIN VPST; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BINDING SITE; BIOFILM; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; QUORUM SENSING; SECOND MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIBRIO CHOLERAE;

CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; QUORUM SENSING; TRANS-ACTIVATORS; VIBRIO CHOLERAE;

VIBRIO CHOLERAE;

EID: 80655125443     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05167-11     Document Type: Article

References (50)

1. Benjaminson, M., B. de Guzman, and A. Weil. 1964. Voges-Proskauer test: expeditious techniques for routine use. J. Bacteriol. 87:234.
2. Beyhan, S., K. Bilecen, S. Salama, C. Casper-Lindley, and F. Yildiz. 2007. Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J. Bacteriol. 189:388-402.
3. Beyhan, S., A. D. Tischler, A. Camilli, and F. H. Yildiz. 2006. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J. Bacteriol. 188:3600-3613.
4. Bobrov, A. G., et al. 2011. Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol. Microbiol. 79:533-551.
5. Brinkman, A., T. Ettema, W. de Vos, and J. van der Oost. 2003. The Lrp family of transcriptional regulators. Mol. Microbiol. 48:287-294.
6. Buck, M., M. T. Gallegos, D. J. Studholme, Y. Guo, and J. D. Gralla. 2000. The bacterial enhancer-dependent sigma 54 (sigma N) transcription factor. J. Bacteriol. 182:4129-4136.
7. Calia, K., M. Murtagh, M. Ferraro, and S. Calderwood. 1994. Comparison of Vibrio cholerae O139 with V. cholerae O1 classical and El Tor biotypes. Infect. Immun. 62:1504-1506.
8. Casper-Lindley, C., and F. Yildiz. 2004. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 186: 1574-1578.
9. Chin, K. H., et al. 2010. The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J. Mol. Biol. 396:646-662.
10. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
11. De, N., M. V. A. S. Navarro, R. V. Raghavan, and H. Sondermann. 2009. Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J. Mol. Biol. 393:619-633.
12. de Lorenzo, V., and K. Timmis. 1994. Analysis and construction of stable phenotypes in Gram-negative bacteria with Tn5-and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
13. Dziejman, M., et al. 2002. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl. Acad. Sci. U. S. A. 99:1556-1561.
14. Fang, X., and M. Gomelsky. 2010. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol. Microbiol. 76:1295-1305.
15. Faruque, S. M., et al. 2006. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. U. S. A. 103:6350-6355.
16. Hammer, B., and B. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101-104.
17. Hammer, B., and B. Bassler. 2007. Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 104:11145-11149.
18. Häse, C., and J. Mekalanos. 1998. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 95:730-734.
19. Hengge, R. 2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7:263-273.
20. Hickman, J., and C. Harwood. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69:376-389.
21. Higgins, D. A., et al. 2007. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883-886.
22. Huq, A., et al. 1983. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45:275-283.
23. Kamruzzaman, M., et al. 2010. Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 107:1588-1593.
24. Kovacikova, G., W. Lin, and K. Skorupski. 2005. Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetate-responsive LysR-type regulator AlsR in Vibrio cholerae. Mol. Microbiol. 57:420-433.
25. Kovacikova, G., W. Lin, and K. Skorupski. 2004. Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Mol. Microbiol. 53:129-142.
26. Kovacikova, G., and K. Skorupski. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:1135-1147.
27. Krasteva, P. V., et al. 2010. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327:866-868.
28. Lim, B., S. Beyhan, J. Meir, and F. H. Yildiz. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60:331-348.
29. Lin, W., G. Kovacikova, and K. Skorupski. 2007. The quorum sensing regulator HapR downregulates the expression of the virulence gene transcription factor AphA in Vibrio cholerae by antagonizing Lrp- and VpsR-mediated activation. Mol. Microbiol. 64:953-967.
30. Long, T., et al. 2009. Quantifying the integration of quorum-sensing signals with single-cell resolution. PLoS Biol. 7:e68.
31. Miller, M., K. Skorupski, D. Lenz, R. Taylor, and B. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303-314.
32. Reddy, C. A., et al. 2007. Methods for general and molecular microbiology, 3rd ed. ASM Press, Washington, DC.
33. Rutherford, S. T., J. C. van Kessel, Y. Shao, and B. L. Bassler. 2011. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev. 25:397-408.
34. Ryjenkov, D. A., R. Simm, U. Romling, and M. Gomelsky. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem. 281:30310-30314.
35. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Skorupski, K., and R. Taylor. 1996. Positive selection vectors for allelic exchange. Gene 169:47-52.
37. Syed, K. A., et al. 2009. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J. Bacteriol. 191:6555-6570.
38. Tamayo, R., J. T. Pratt, and A. Camilli. 2007. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu. Rev. Microbiol. 61:131-148.
39. Tamayo, R., S. Schild, J. Pratt, and A. Camilli. 2008. Role of cyclic di-GMP during El Tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic di-GMP phosphodiesterase CdpA. Infect. Immun. 76: 1617-1627.
40. Tamayo, R., A. Tischler, and A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280:33324-33330.
41. Thelin, K., and R. Taylor. 1996. Toxin-coregulated pilus, but not mannosesensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect. Immun. 64:2853-2856.
42. Tischler, A., and A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
43. Van Houdt, R., A. Aertsen, and C. W. Michiels. 2007. Quorum-sensingdependent switch to butanediol fermentation prevents lethal medium acidification in Aeromonas hydrophila AH-1N. Res. Microbiol. 158:379-385.
44. Waters, C., and B. Bassler. 2006. The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev. 20:2754-2767.
45. Waters, C., W. Lu, J. Rabinowitz, and B. Bassler. 2008. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J. Bacteriol. 190:2527-2536.
46. Waters, C. M., and B. L. Bassler. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21:319-346.
47. Yang, M., E. M. Frey, Z. Liu, R. Bishar, and J. Zhu. 2010. The virulence transcriptional activator AphA enhances biofilm formation by Vibrio cholerae by activating expression of the biofilm regulator VpsT. Infect. Immun. 78: 697-703.
48. Yildiz, F., N. Dolganov, and G. Schoolnik. 2001. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPSETr-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183:1716-1726. 11160103.
49. Yildiz, F., and G. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 96:4028-4033.
50. Zhu, J., and J. Mekalanos. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5:647-656.