Mutations in the extracellular protein secretion pathway genes (eps) interfere with rugose polysaccharide production in and motility of Vibrio cholerae

Infection and Immunity

Volumn 68, Issue 4, 2000, Pages 1967-1974

  Ali, Afsar ^a   Johnson, Judith A ^a,b   Franco, Augusto A ^c   Metzger, Daniel J ^d   Connell, Terry D ^d   Morris Jr , J Glenn ^a,b   Sozhamannan, Shanmuga ^a,b  

^a Division of Hospital Epidemiology   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c Division of Emergency Medicine   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHLORINE;

ARTICLE; BIOFILM; GENE MUTATION; MOLECULAR CLONING; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; SEQUENCE ANALYSIS; VIBRIO CHOLERAE;

ALKALINE PHOSPHATASE; BACTERIAL PROTEINS; CHOLERA TOXIN; CLONING, MOLECULAR; COSMIDS; CYCLIN-DEPENDENT KINASES; FLAGELLA; GENETIC COMPLEMENTATION TEST; HEMOLYSIN PROTEINS; MEMBRANE PROTEINS; MOVEMENT; MUTAGENESIS; MUTATION; OPERON; PHENOTYPE; POLYSACCHARIDES; VIBRIO CHOLERAE;

EID: 0034018022     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.4.1967-1974.2000     Document Type: Article

References (52)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Beck von Bodman, S., and S. K. Farrand. 1995. Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J. Bacteriol. 177:5009-5008.
3. Berg, D. E. 1989. Transposon Tn5, p. 185-210. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
4. Cameron, D. N., F. M. Khambaty, I. K. Wachsmuth, R. V. Tauxe, and T. J. Barrett. 1994. Molecular characterization of Vibrio cholerae O1 strains by pulsed-field gel electrophoresis. J. Clin. Microbiol. 32:1685-1690.
5. Connell, T. D., D. J. Metzger, M. Wang, M. G. Jobling, and R. K. Holmes. 1995. Initial studies of the structural signal for extracellular transport of cholera toxin and other proteins recognized by Vibrio cholerae. Infect. Immun. 63:4091-4098.
6. Costa, J. M., and J. E. Loper. 1997. EcbI and EcbR: homologs of LuxI and LuxR affecting antibiotic and exoenzyme production by Erwinia carotovora subsp. betavasculorum. Can. J. Microbiol. 43:1164-1171.
7. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive selection suicide vector. Infect. Immun. 59:4310-4317.
8. Glass, R. I., M. Claeson, P. A. Blake, R. J. Waldman, and N. F. Pierce. 1991. Cholera in Africa: lessons on transmission and control for Latine America. Lancet 338:791-795.
9. Hardie, K. R., S. Lory, and A. P. Pugsley. 1996. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15:978-988.
10. Hassett, D. J., J. F. Ma, J. G. Elkins, T. R. McDermott, U. A. Ochsner, S. E. West, C. T. Huang, J. Fredericks, S. Burnett, P. S. Stewart, G. McFeters, L. Passador, and B. H. Iglewski. 1999. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol. Microbiol. 34: 1082-1093.
11. Hohn, B., and J. Collins. 1980. A small cosmid for efficient cloning of large DNA fragments. Gene 11:291-298.
12. Holmes, R. K., M. L. Vasil, and R. A. Finkelstein. 1975. Studies on toxinogenesis in Vibrio cholerae. III. Characterization of nontoxinogenic mutants in vitro and in experimental animals. J. Clin. Invest. 55:551-560.
13. Islam, M. S., B. S. Drasar, and R. B. Sack. 1994. The aquatic flora and fauna as reservoirs of Vibrio cholerae: a review. J. Diarrhoeal Dis. Res. 12:87-96.
14. Jobling, M. G., and R. K. Holmes. 1997. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol. Microbiol. 26:1023-1034.
15. Kaper, J. B., J. G. Morris, Jr., and M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8:48-86.
16. Karaolis, D. K., S. Somara, D. R. Maneval, Jr., J. A. Johnson, and J. B. Kaper. 1999. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399:375-379.
17. Klose, K. E., and J. J. Mekalanos. 1998. Differential regulation of multiple flagellins in Vibrio cholerae. J. Bacteriol. 180:303-316.
18. Klose, K. E., and J. J. Mekalanos. 1998. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 28:501-520.
19. Kornacker, M. G., and A. P. Pugsley. 1990. Molecular characterization of pulA and its product, pullulanase, a secreted enzyme of Klebsiella pneumoniae UNF5023. Mol. Microbiol. 4:73-85.
20. Latifi, A., M. K. Winson, M. Foglino, B. W. Bycroft, G. S. Stewart, A. Lazdunski, and P. Williams. 1995. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 17:333-343.
21. Lindeberg, M., and A. Collmer. 1992. Analysis of eight out genes in a cluster required for pectic enzyme secretion by Erwinia chrysanthemi: sequence comparison with secretion genes from other gram-negative bacteria. J. Bacteriol. 174:7385-7397.
22. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
23. Manoil, C., and J. Beckwith. 1985. TnphoA: a transposon probe for protein export signals. Proc. Natl. Acad. Sci. USA 82:8129-8133.
24. Marsh, J. W., and R. K. Taylor. 1998. Identification of the Vibrio cholerae type 4 prepilin peptidase required for cholera toxin secretion and pilus formation. Mol. Microbiol. 29:1481-1492.
25. Martin, P. R., M. Hobbs, P. D. Free, Y. Jeske, and S. J. Mattick. 1993. Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol. 9:857-868.
26. Menard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
27. Metcalf, W. W., and B. L. Wanner. 1993. Construction of new beta-glucuronidase cassettes for making transcriptional fusions and their use with new methods for allele replacement. Gene 129:17-25.
28. Morris, J. G., Jr., M. B. Sztein, E. W. Rice, J. P. Nataro, G. A. Losonsky, P. Panigrahi, C. O. Tacket, and J. A. Johnson. 1996. Vibrio cholerae O1 can assume a chlorine-resistant rugose survival form that is virulent for humans. J. Infect. Dis. 174:1364-1368.
29. Nagamune, K., K. Yamamoto, A. Naka, J. Matsuyama, T. Miwatani, and T. Honda. 1996. In vitro proteolytic processing and activation of the recombinant precursor of El Tor cytolysin/hemolysin (pro-HlyA) of Vibrio cholerae by soluble hemagglutinin/protease of V. cholerae, trypsin, and other proteases. Infect. Immun. 64:4655-4658.
30. Overbye, L. J., M. Sandkvist, and M. Bagdasarian. 1993. Genes required for extracellular secretion of enterotoxin are clustered in Vibrio cholerae. Gene 132:101-106.
31. Pal, S. C. 1992. Laboratory diagnosis, p. 229-251. In D. Barua and W. B. Greenough III (ed.), Cholera. Plenum Medical Book Co., New York, N.Y.
32. Pugsley, A. P. 1993. The complete general secretory pathway in Gram-negative bacteria. Microbiol. Rev. 57:50-108.
33. Reeves, P. J., D. Whitcombe, S. Wharam, M. Gibson, G. Allison, N. Bunce, R. Barallon, P. Douglas, V. Mulholland, S. Stevens, D. Walker, and G. P. C. Salmond. 1993. Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: genes encoding members of a general secretion pathway (GSP) widespread in Gram-negative bacteria. Mol. Microbiol. 8:443-456.
34. Rice, E. W., C. H. Johnson, R. M. Clark, K. R. Fox, D. J. Reasoner, M. E. Dunnigan, P. Panigrahi, J. A. Johnson, and J. G. Morris Jr. 1993. Vibrio cholerae O1 can assume a "rugose" survival form that resists killing by chlorine, yet retains virulence. Int. J. Environ. Health Res. 3:89-98.
35. Roszak, D. B., and R. R. Colwell. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:365-379.
36. Russel, M. 1994. Phage assembly: a paradigm for bacterial virulence factor export? Science 265:612-614.
37. Russel, M. 1998. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J. Mol. Biol. 279:485-499.
38. Sandkvist, M., V. Morales, and M. Bagdasarian. 1993. A protein required for secretion of cholera toxin through the outer membrane of Vibrio cholerae. Gene 123:81-86.
39. Sandkvist, M., M. Bagdasarian, S. P. Howard, and V. J. DiRita. 1995. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in V. cholerae. EMBO J. 14: 1664-1673.
40. Sandkvist, M., L. O. Michel, L. P. Hough, V. M. Morales, M. Bagdasarian, M. Koomey, V. J. DiRita, and M. Bagdasarian. 1997. General secretion pathway (eps) genes required for toxin secretion and outer membrane biogenesis in Vibrio cholerae. J. Bacteriol. 179:6994-7003.
41. Sandkvist, M., L. P. Hough, M. M. Bagdasarian, and M. Bagdasarian. 1999. Direct interaction of the EpsL and EpsM proteins of the general secretion apparatus in Vibrio cholerae. J. Bacteriol. 181:3129-3135.
42. Shiba, T., R. T. Hill, W. L. Straube, and R. R. Colwell. 1995. Decrease in culturability of Vibrio cholerae caused by glucose. Appl. Environ. Microbiol. 61:2583-2588.
43. Taylor, R. K., C. Manoil, and J. J. Mekalanos. 1989. Broad-host-range vectors for delivery of TnphoA: use in genetic analysis of secreted virulence determinants of Vibrio cholerae. J. Bacteriol. 171:1870-1878.
44. Thomas, S. R., and T. J. Trust. 1995. A specific PulD homolog is required for the secretion of paracrystalline surface array subunits in Aeromonas hydrophila. J. Bacteriol. 177:3932-3939.
45. Wai, S. N., Y. Mizunoe, A. Takade, S.-I. Kawabata, and S.-I. Yoshida. 1998. Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl. Environ. Microbiol. 64:3648-3655.
46. Wai, S. N., Y. Mizunoe, and S.-I. Yoshida. 1999. How Vibrio cholerae survive during starvation. FEMS Microbiol. Lett. 180:123-131.
47. Watnick, P. I., K. J. Fullner, and R. Kolter. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181:3606-3609.
48. Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586-595.
49. White, P. B. 1938. The rugose variant of vibrios. J. Pathol. Bacteriol. 46:1-6.
50. White, P. B. 1940. The characteristic hapten and antigen of rugose races of cholera and El Tor vibrios. J. Pathol. Bacteriol. 50:160-164.
51. Yamamoto, K., Y. Ichinose, H. Shinagawa, K. Makino, A. Nakata, M. Iwanaga, T. Honda, and T. Miwatani. 1990. Two-step processing for activation of the cytolysin/hemolysin of Vibrio cholerae O1 biotype El Tor: nucleotide sequence of the structural gene (hlyA) and characterization of the processed products. Infect. Immun. 58:4106-4116.
52. 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. USA 96:4028-4033.