The phosphoenolpyruvate phosphotransferase system regulates Vibrio cholerae biofilm formation through multiple independent pathways

Journal of Bacteriology

Volumn 192, Issue 12, 2010, Pages 3055-3067

  Houot, Laetitia ^a,b   Chang, Sarah ^a   Pickering, Bradley S ^a   Absalon, Cedric ^a   Watnick, Paula I ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; GLUCOSE; HISTIDINE; NITROGEN; PHOSPHOENOLPYRUVATE PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE; PYRUVIC ACID; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM; BIOFILM; BROTH DILUTION; CELL FUNCTION; CULTURE MEDIUM; CYTOPLASM; ENVIRONMENT; ENVIRONMENTAL FACTOR; ENZYME SPECIFICITY; GENE STRUCTURE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SURFACE PROPERTY; VIBRIO CHOLERAE; VIRULENCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PHOSPHORYLATION; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE;

EID: 77954001197     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00213-10     Document Type: Article

References (64)

1. Abranches, J., M. M. Candella, Z. T. Wen, H. V. Baker, and R. A. Burne. 2006. Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans. J. Bacteriol. 188:3748-3756.
2. Barriere, C., M. Veiga-da-Cunha, N. Pons, E. Guedon, S. A. van Hijum, J. Kok, O. P. Kuipers, D. S. Ehrlich, and P. Renault. 2005. Fructose utilization in Lactococcus lactis as a model for low-GC gram-positive bacteria: its regulator, signal, and DNA-binding site. J. Bacteriol. 187:3752-3761.
3. Berg, T., S. Schild, and J. Reidl. 2007. Regulation of the chitobiose-phosphotransferase system in Vibrio cholerae. Arch. Microbiol. 187:433-439.
4. Beyhan, S., and F. H. Yildiz. 2007. Smooth to rugose phase variation in Vibrio cholerae can be mediated by a single nucleotide change that targets c-di-GMP signalling pathway. Mol. Microbiol. 63:995-1007.
5. Bomchil, N., P. Watnick, and R. Kolter. 2003. Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J. Bacteriol. 185:1384-1390.
6. Bonet, R., M. D. Simon-Pujol, and F. Congregado. 1993. Effects of nutrients on exopolysaccharide production and surface properties of Aeromonas salmonicida. Appl. Environ. Microbiol. 59:2437-2441.
7. Branda, S. S., S. Vik, L. Friedman, and R. Kolter. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13:20-26.
8. Colwell, R. R., and A. Huq. 1994. Environmental reservoir of Vibrio cholerae. The causative agent of cholera. Ann. N. Y. Acad. Sci. 740:44-54.
9. De Kievit, T. R., R. Gillis, S. Marx, C. Brown, and B. H. Iglewski. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67:1865-1873.
10. Deutscher, J., C. Francke, and P. W. Postma. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70:939-1031.
11. Fong, J. C., and F. H. Yildiz. 2008. Interplay between cyclic AMP-cyclic AMP receptor protein and cyclic di-GMP signaling in Vibrio cholerae biofilm formation. J. Bacteriol. 190:6646-6659.
12. Gershanovitch, V. N., N. V. Yourovitskaya, L. V. Komissarova, T. N. Bolshakova, R. S. Erlagaeva, and G. I. Bourd. 1975. Catabolite repression in Escherichia coli K12 mutants defective in glucose transport. Mol. Gen. Genet. 140:81-90.
13. Hammer, B. K., and B. L. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101-104.
14. Hang, L., M. John, M. Asaduzzaman, E. A. Bridges, C. Vanderspurt, T. J. Kirn, R. K. Taylor, J. D. Hillman, A. Progulske-Fox, M. Handfield, E. T. Ryan, and S. B. Calderwood. 2003. Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 100:8508-8513.
15. Haugo, A. J., and P. I. Watnick. 2002. Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 45:471-483.
16. Houot, L., S. Chang, C. Absalon, and P. I. Watnick. 2010. Vibrio cholerae phosphoenolpyruvate phosphotransferase system control of carbohydrate transport, biofilm formation, and colonization of the germfree mouse intestine. Infect. Immun. 78:1482-1494.
17. Houot, L., and P. I. Watnick. 2008. A novel role for enzyme I of the Vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm. J. Bacteriol. 190:311-320.
18. Karatan, E., T. R. Duncan, and P. I. Watnick. 2005. NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J. Bacteriol. 187:7434-7443.
19. Karatan, E., and P. Watnick. 2009. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol. Mol. Biol. Rev. 73:310-347.
20. Kierek, K., and P. I. Watnick. 2003. Environmental determinants of Vibrio cholerae biofilm development. Appl. Environ. Microbiol. 69:5079-5088.
21. Kim, S. Y., T. W. Nam, D. Shin, B. M. Koo, Y. J. Seok, and S. Ryu. 1999. Purification of Mlc and analysis of its effects on the pts expression in Escherichia coli. J. Biol. Chem. 274:25398-25402.
22. King, N. D., and M. R. O'Brian. 2001. Evidence for direct interaction between enzyme I(Ntr) and aspartokinase to regulate bacterial oligopeptide transport. J. Biol. Chem. 276:21311-21316.
23. Lauriano, C. M., C. Ghosh, N. E. Correa, and K. E. Klose. 2004. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J. Bacteriol. 186:4864-4874.
24. + transporter TrkA. Proc. Natl. Acad. Sci. U. S. A. 104:4124-4129.
25. Lee, C. R., B. M. Koo, S. H. Cho, Y. J. Kim, M. J. Yoon, A. Peterkofsky, and Y. J. Seok. 2005. Requirement of the dephospho-form of enzyme IIANtr for derepression of Escherichia coli K-12 ilvBN expression. Mol. Microbiol. 58:334-344.
26. Lee, J., A. Jayaraman, and T. K. Wood. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7:42.
27. Lee, S. J., W. Boos, J. P. Bouche, and J. Plumbridge. 2000. Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J. 19:5353-5361.
28. Liang, W., A. J. Silva, and J. A. Benitez. 2007. The cyclic AMP receptor protein modulates colonial morphology in Vibrio cholerae. Appl. Environ. Microbiol. 73:7482-7487.
29. Lim, B., S. Beyhan, and F. H. Yildiz. 2007. Regulation of Vibrio polysaccharide synthesis and virulence factor production by CdgC, a GGDEF-EAL domain protein, in Vibrio cholerae. J. Bacteriol. 189:717-729.
30. Lombardo, M. J., J. Michalski, H. Martinez-Wilson, C. Morin, T. Hilton, C. G. Osorio, J. P. Nataro, C. O. Tacket, A. Camilli, and J. B. Kaper. 2007. An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers. Proc. Natl. Acad. Sci. U. S. A. 104:18229-18234.
31. Loo, C. Y., K. Mitrakul, I. B. Voss, C. V. Hughes, and N. Ganeshkumar. 2003. Involvement of an inducible fructose phosphotransferase operon in Streptococcus gordonii biofilm formation. J. Bacteriol. 185:6241-6254.
32. Mao, X. J., Y. X. Huo, M. Buck, A. Kolb, and Y. P. Wang. 2007. Interplay between CRP-cAMP and PII-Ntr systems forms novel regulatory network between carbon metabolism and nitrogen assimilation in Escherichia coli. Nucleic Acids Res. 35:1432-1440.
33. Martino, P. D., R. Fursy, L. Bret, B. Sundararaju, and R. S. Phillips. 2003. Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can. J. Microbiol. 49:443-449.
34. Matson, J. S., J. H. Withey, and V. J. DiRita. 2007. Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect. Immun. 75:5542-5549.
35. McGinnis, M. W., Z. M. Parker, N. E. Walter, A. C. Rutkovsky, C. Cartaya-Marin, and E. Karatan. 2009. Spermidine regulates Vibrio cholerae biofilm formation via transport and signaling pathways. FEMS Microbiol. Lett.
36. Michiels, J., T. Van Soom, I. D'Hooghe, B. Dombrecht, T. Benhassine, P. de Wilde, and J. Vanderleyden. 1998. The Rhizobium etli rpoN locus: DNA sequence analysis and phenotypical characterization of rpoN, ptsN, and ptsA mutants. J. Bacteriol. 180:1729-1740.
37. Miller, M. B., K. Skorupski, D. H. Lenz, R. K. Taylor, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303-314.
38. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
39. Mitchell, W. J., T. P. Misko, and S. Roseman. 1982. Sugar transport by the bacterial phosphotransferase system. Regulation of other transport systems (lactose and melibiose). J. Biol. Chem. 257:14553-14564.
40. Moorthy, S., and P. I. Watnick. 2004. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol. Microbiol. 52:573-587.
41. Mueller, R. S., S. Beyhan, S. G. Saini, F. H. Yildiz, and D. H. Bartlett. 2009. Indole acts as an extracellular cue regulating gene expression in Vibrio cholerae. J. Bacteriol. 191:3504-3516.
42. Munoz-Elias, E. J., J. Marcano, and A. Camilli. 2008. Isolation of Streptococcus pneumoniae biofilm mutants and their characterization during nasopharyngeal colonization. Infect. Immun. 76:5049-5061.
43. Nam, T. W., H. I. Jung, Y. J. An, Y. H. Park, S. H. Lee, Y. J. Seok, and S. S. Cha. 2008. Analyses of Mlc-IIBGlc interaction and a plausible molecular mechanism of Mlc inactivation by membrane sequestration. Proc. Natl. Acad. Sci. U. S. A. 105:3751-3756.
44. Noguez, R., D. Segura, S. Moreno, A. Hernandez, K. Juarez, and G. Espin. 2008. Enzyme I NPr, NPr and IIA Ntr are involved in regulation of the poly-beta-hydroxybutyrate biosynthetic genes in Azotobacter vinelandii. J. Mol. Microbiol. Biotechnol. 15:244-254.
45. Patel, C. N., B. W. Wortham, J. L. Lines, J. D. Fetherston, R. D. Perry, and M. A. Oliveira. 2006. Polyamines are essential for the formation of plague biofilm. J. Bacteriol. 188:2355-2363.
46. Pfluger, K., and V. de Lorenzo. 2008. Evidence of in vivo cross talk between the nitrogen-related and fructose-related branches of the carbohydrate phosphotransferase system of Pseudomonas putida. J. Bacteriol. 190:3374-3380.
47. Plumbridge, J. 1998. Control of the expression of the manXYZ operon in Escherichia coli: Mlc is a negative regulator of the mannose PTS. Mol. Microbiol. 27:369-380.
48. Powell, B. S., D. L. Court, T. Inada, Y. Nakamura, V. Michotey, X. Cui, A. Reizer, M. H. Saier, Jr., and J. Reizer. 1995. Novel proteins of the phosphotransferase system encoded within the rpoN operon of Escherichia coli. Enzyme IIANtr affects growth on organic nitrogen and the conditional lethality of an erats mutant. J. Biol. Chem. 270:4822-4839.
49. Reizer, J., A. Reizer, M. J. Lagrou, K. R. Folger, C. K. Stover, and M. H. Saier, Jr. 1999. Novel phosphotransferase systems revealed by bacterial genome analysis: the complete repertoire of pts genes in Pseudomonas aeruginosa. J. Mol. Microbiol. Biotechnol. 1:289-293.
50. Reizer, J., A. Reizer, M. J. Merrick, G. Plunkett III, D. J. Rose, and M. H. Saier, Jr. 1996. Novel phosphotransferase-encoding genes revealed by analysis of the Escherichia coli genome: a chimeric gene encoding an enzyme I homologue that possesses a putative sensory transduction domain. Gene 181:103-108.
51. Ren, J., S. Sainsbury, N. S. Berrow, D. Alderton, J. E. Nettleship, D. K. Stammers, N. J. Saunders, and R. J. Owens. 2005. Crystal structure of nitrogen regulatory protein IIANtr from Neisseria meningitidis. BMC Struct. Biol. 5:13.
52. Saier, M. H., Jr. 1989. Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate:sugar phosphotransferase system. Microbiol. Rev. 53:109-120.
53. Seidl, K., C. Goerke, C. Wolz, D. Mack, B. Berger-Bachi, and M. Bischoff. 2008. Staphylococcus aureus CcpA affects biofilm formation. Infect. Immun. 76:2044-2050.
54. Seok, Y. J., B. M. Koo, M. Sondej, and A. Peterkofsky. 2001. Regulation of E. coli glycogen phosphorylase activity by HPr. J. Mol. Microbiol. Biotechnol. 3:385-393.
55. Seok, Y. J., M. Sondej, P. Badawi, M. S. Lewis, M. C. Briggs, H. Jaffe, and A. Peterkofsky. 1997. High affinity binding and allosteric regulation of Escherichia coli glycogen phosphorylase by the histidine phosphocarrier protein, HPr. J. Biol. Chem. 272:26511-26521.
56. Stulke, J., and W. Hillen. 1998. Coupling physiology and gene regulation in bacteria: the phosphotransferase sugar uptake system delivers the signals. Naturwissenschaften 85:583-592.
57. Tamayo, R., A. D. Tischler, and A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280:33324-33330.
58. Tanaka, Y., K. Kimata, and H. Aiba. 2000. A novel regulatory role of glucose transporter of Escherichia coli: membrane sequestration of a global repressor Mlc. EMBO J. 19:5344-5352.
59. Tanaka, Y., K. Kimata, T. Inada, H. Tagami, and H. Aiba. 1999. Negative regulation of the pts operon by Mlc: mechanism underlying glucose induction in Escherichia coli. Genes Cells 4:391-399.
60. Titgemeyer, F. 1993. Signal transduction in chemotaxis mediated by the bacterial phosphotransferase system. J. Cell Biochem. 51:69-74.
61. Van Dellen, K. L., L. Houot, and P. I. Watnick. 2008. Genetic analysis of Vibrio cholerae monolayer formation reveals a key role for Δψ 32 ιn the transition to permanent attachment. J. Bacteriol. 190:8185-8196.
62. Velazquez, F., K. Pfluger, I. Cases, L. I. De Eugenio, and V. de Lorenzo. 2007. The phosphotransferase system formed by PtsP, PtsO, and PtsN proteins controls production of polyhydroxyalkanoates in Pseudomonas putida. J. Bacteriol. 189:4529-4533.
63. Watnick, P. I., C. M. Lauriano, K. E. Klose, L. Croal, and R. Kolter. 2001. Absence of a flagellum leads to altered colony morphology, biofilm development, and virulence in V. cholerae O139. Mol. Microbiol. 39:223-235.
64. Yildiz, F. H., and G. K. 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.