Vibrio cholerae phosphoenolpyruvate phosphotransferase system control of carbohydrate transport, biofilm formation, and colonization of the germfree mouse intestine

Infection and Immunity

Volumn 78, Issue 4, 2010, Pages 1482-1494

  Houot, Laetitia ^a   Chang, Sarah ^a   Absalon, Cedric ^a   Watnick, Paula I ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; PHOSPHOENOLPYRUVATE; PHOSPHOTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BIOFILM; CARBOHYDRATE TRANSPORT; CONTROLLED STUDY; FEMALE; GERMFREE ANIMAL; IN VITRO STUDY; INTESTINE; LARGE INTESTINE; LIFE CYCLE; MAMMAL; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SMALL INTESTINE; VIBRIO CHOLERAE;

ANIMALS; BIOFILMS; CARBOHYDRATE METABOLISM; COLONY COUNT, MICROBIAL; FEMALE; INTESTINES; MICE; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; VIBRIO CHOLERAE;

EID: 77950206096     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01356-09     Document Type: Article

References (40)

1. Berg, T., S. Schild, and J. Reidl. 2007. Regulation of the chitobiose-phosphotransferase system in Vibrio cholerae. Arch. Microbiol. 187:433-439.
2. Brown, J. H., and L. Brenn. 1931. A method for the differential staining of Gram-positive and Gram-negative bacteria in tissue sections. Bull. Johns Hopkins Hosp. 48:69-73.
3. Butterton, J. R., E. T. Ryan, R. A. Shahin, and S. B. Calderwood. 1996. Development of a germfree mouse model of Vibrio cholerae infection. Infect. Immun. 64:4373-4377.
4. Chiang, S. L., and J. J. Mekalanos. 1998. Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Mol. Microbiol. 27:797-805.
5. 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.
6. Faruque, S. M., and G. B. Nair. 2002. Molecular ecology of toxigenic Vibrio cholerae. Microbiol. Immunol. 46:59-66.
7. 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.
8. Haugo, A. J., and P. I. Watnick. 2002. Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 45:471-483.
9. Herrington, D. A., R. H. Hall, G. Losonsky, J. J. Mekalanos, R. K. Taylor, and M. M. Levine. 1988. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168: 1487-1492.
10. Hogema, B. M., J. C. Arents, R. Bader, K. Eijkemans, H. Yoshida, H. Takahashi, H. Aiba, and P. W. Postma. 1998. Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mol. Microbiol. 30:487-498.
11. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
12. 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.
13. Kierek, K., and P. I. Watnick. 2003. Environmental determinants of Vibrio cholerae biofilm development. Appl. Environ. Microbiol. 69:5079-5088.
14. Kok, M., G. Bron, G. Erni, and S. Mukhija. 2003. Effect of enzyme I of the bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS) on virulence in a murine model. Microbiology 149:2645-2652.
15. Kornberg, H. 1986. The roles of HPr and FPr in the utilization of fructose by Escherichia coli. FEBS Lett. 194:12-15.
16. Larsen, M. H., B. H. Kallipolitis, J. K. Christiansen, J. E. Olsen, and H. Ingmer. 2006. The response regulator ResD modulates virulence gene expression in response to carbohydrates in Listeria monocytogenes. Mol. Microbiol. 61:1622-1635.
17. 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.
18. 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.
19. Merrell, D. S., D. L. Hava, and A. Camilli. 2002. Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol. Microbiol. 43:1471-1491.
20. Metcalf, W. W., W. Jiang, L. L. Daniels, S. K. Kim, A. Haldimann, and B. L. Wanner. 1996. Conditionally replicative and conjugative plasmids carrying lacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35:1-13.
21. 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.
22. Moorthy, S., and P. I. Watnick. 2005. Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol. Microbiol. 57:1623-1635.
23. Nygren, E., B. L. Li, J. Holmgren, and S. R. Attridge. 2009. Establishment of an adult mouse model for direct evaluation of the efficacy of vaccines against Vibrio cholerae. Infect. Immun. 77:3475-3484.
24. Olivier, V., J. Queen, and K. J. Satchell. 2009. Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins. PLoS One 4:e7352.
25. Olivier, V., N. H. Salzman, and K. J. Satchell. 2007. Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins. Infect. Immun. 75:5043-5051.
26. 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.
27. Poncet, S., E. Milohanic, A. Maze, J. N. Abdallah, F. Ake, M. Larribe, A. E. Deghmane, M. K. Taha, M. Dozot, X. De Bolle, J. J. Letesson, and J. Deutscher. 2009. Correlations between carbon metabolism and virulence in bacteria. Contrib. Microbiol. 16:88-102.
28. Postma, P. W., J. W. Lengeler, and G. R. Jacobson. 1993. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57:543-594.
29. Rabus, R., J. Reizer, I. Paulsen, and M. H. Saier, Jr. 1999. Enzyme I(Ntr) from Escherichia coli. A novel enzyme of the phosphoenolpyruvate- dependent phosphotransferase system exhibiting strict specificity for its phosphoryl acceptor, NPr. J. Biol. Chem. 274:26185-26191.
30. 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.
31. Rouquet, G., G. Porcheron, C. Barra, M. Reperant, N. K. Chanteloup, C. Schouler, and P. Gilot. 2009. A metabolic operon in extraintestinal pathogenic Escherichia coli promotes fitness under stressful conditions and invasion of eukaryotic cells. J. Bacteriol. 191:4427-4440.
32. Sack, R. B., and C. E. Miller. 1969. Progressive changes of vibrio serotypes in germ-free mice infected with Vibrio cholerae. J. Bacteriol. 99:688-695.
33. Shemesh, M., A. Tam, and D. Steinberg. 2007. Expression of biofilm-associated genes of Streptococcus mutans in response to glucose and sucrose. J. Med. Microbiol. 56:1528-1535.
34. Stulke, J. 2007. Regulation of virulence in Bacillus anthracis: the phosphotransferase system transmits the signals. Mol. Microbiol. 63:626-628.
35. Taylor, R. K., V. L. Miller, D. B. Furlong, and J. J. Mekalanos. 1986. Identification of a pilus colonization factor that is coordinately regulated with cholera toxin. Ann. Sclavo Collana Monogr. 3:51-61.
36. Thelin, K. H., and R. K. Taylor. 1996. Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect. Immun. 64:2853-2856.
37. Van Dellen, K. L., L. Houot, and P. I. Watnick. 2008. Genetic analysis of Vibrio cholerae monolayer formation reveals a key role for Δψ in the transition to permanent attachment. J. Bacteriol. 190:8185-8196.
38. 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.
39. Yildiz, F. H., N. A. Dolganov, and G. K. Schoolnik. 2001. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183:1716-1726.
40. Yildiz, F. H., and G. K. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identi- fication 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.