Vibrio fischeri flagellin A is essential for normal motility and for symbiotic competence during initial squid light organ colonization

Journal of Bacteriology

Volumn 186, Issue 13, 2004, Pages 4315-4325

  Millikan, Deborah S ^a   Ruby, Edward G ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLAGELLIN; PROTEIN FLAF; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIUM MUTANT; CELL MOTILITY; FLAA GENE; FLAC GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; SQUID; SYMBIOSIS; VIBRIO FISCHERI;

ANIMALS; CHROMOSOME MAPPING; DECAPODIFORMES; FLAGELLIN; LIGHT; MOVEMENT; SYMBIOSIS; VIBRIO;

ANIMALIA; BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA; EUPRYMNA SCOLOPES; HAWAIIA; NEGIBACTERIA; PHOTOBACTERIUM; SCOLOPES; VIBRIO; VIBRIO FISCHERI;

EID: 3042611950     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.13.4315-4325.2004     Document Type: Article

References (50)

1. Akerley, B. J., D. M. Monack, S. Falkow, and J. F. Miller. 1992. The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J. Bacteriol. 174:980-990.
2. Allen, R. D., and P. Baumann. 1971. Structure and arrangement of flagella in species of the genus Beneckea and Photobacterium fischeri. J. Bacteriol. 107:295-302.
3. Arora, S. K., B. W. Ritchings, E. C. Almira, S. Lory, and R. Ramphal. 1997. A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J. Bacteriol. 179:5574-5581.
4. Arora, S. K., B. W. Ritchings, E. C. Almira, S. Lory, and R. Ramphal. 1998. The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect. Immun. 66:1000-1007.
5. Barrios, H., B. Valderrama, and E. Morett. 1999. Compilation and analysis of sigma (54)-dependent promoter sequences. Nucleic Acids Res. 27:4305-4313.
6. Boettcher, K. J., and E. G. Ruby. 1990. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172:3701-3706.
7. Brimer, C. D., and T. C. Montie. 1998. Cloning and comparison of fliC genes and identification of glycosylation in the flagellin of Pseudomonas aeruginosa a-type strains. J. Bacteriol. 180:3209-3217.
8. Clyne, M., T. Ocroinin, S. Suerbaum, C. Josenhans, and B. Drumm. 2000. Adherence of isogenic flagellum-negative mutants of Helicobacter pylori and Helicobacter mustelae to human and ferret gastric epithelial cells. Infect. Immun. 68:4335-4339.
9. Deakin, W. J., V. E. Parker, E. L. Wright, K. J. Ashcroft, G. J. Loake, and C. H. Shaw. 1999. Agrobacterium tumefaciens possesses a fourth flagellin gene located in a large gene cluster concerned with flagellar structure, assembly and motility. Microbiology 145:1397-1407.
10. DeLoney-Marino, C. R., A. J. Wolfe, and K. L. Visick. 2003. Chemoattraction of Vibrio fischeri to serine, nucleosides and N-acetylneuraminic acid, a component of squid light organ mucus. Appl. Environ. Microbiol. 69:7527-7530.
11. Doino Lemus, J., and M. J. McFall-Ngai. 2000. Alterations in the proteome of the Euprymna scolopes light organ in response to symbiotic Vibrio fischeri. Appl. Environ. Microbiol. 66:4091-4097.
12. Driks, A., R. Bryan, L. Shapiro, and D. J. DeRosier. 1989. The organization of the Caulobacter crescentus flagellar filament. J. Mol. Biol. 206:627-636.
13. Graf, J., P. V. Dunlap, and E. G. Ruby. 1994. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J. Bacteriol. 176:6986-6991.
14. Graf, J., and E. G. Ruby. 1998. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl. Acad. Sci. USA 95:1818-1822.
15. Guerry, P., S. M. Logan, S. Thornton, and T. J. Trust. 1990. Genomic organization and expression of Campylobacter flagellin genes. J. Bacteriol. 172:1853-1860.
16. Helmann, J. D., and M. J. Chamberlin. 1987. DNA sequence analysis suggests that expression of flagellar and chemotaxis genes in Escherichia coli and Salmonella typhimurium is controlled by an alternative sigma factor. Proc. Natl. Acad. Sci. USA 84:6422-6424.
17. Jacchieri, S. G., R. Torquato, and R. R. Brentani. 2003. Structural study of binding of flagellin by Toll-like receptor 5. J. Bacteriol. 185:4243-4247.
18. Josenhans, C., R. L. Ferrero, A. Labigne, and S. Suerbaum. 1999. Cloning and allelic exchange mutagenesis of two flagellin genes of Helicobacter felis. Mol. Microbiol. 33:350-362.
19. Kapatral, V., and S. A. Minnich. 1995. Coordinate temperature-sensitive regulation of transcription of three Yersinia enterocolitica flagellin genes. Mol. Microbiol. 17:49-56.
20. Kelly-Wintenberg, K., T. Anderson, and T. C. Montie. 1990. Phosphorylated tyrosines in the flagellum filament protein of Pseudomonas aeruginosa. J. Bacteriol. 172:5135-5139.
21. Kim, Y. K., and L. L. McCarter. 2000. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 182:3693-3704.
22. Kimbell, J., and M. McFall-Ngai. 2003. The squid-vibrio symbioses: from demes to genes. Integ. Comp. Biol. 43:254-260.
23. Klose, K. E., and J. J. Mekalanos. 1998. Differential regulation of multiple flagellins in Vibrio cholerae. J. Bacteriol. 180:303-316.
24. Logan, S. M., T. J. Trust, and P. Guerry. 1989. Evidence for posttranslational modification and gene duplication of Campylobacter flagellin. J. Bacteriol. 171:3031-3038.
25. McCann, J. R., E. V. Stabb, D. S. Millikan, and E. G. Ruby. 2003. Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Appl. Environ. Microbiol. 69:5928-5934.
26. McCarter, L. L. 1995. Genetic and molecular characterization of the polar flagellum of Vibrio parahaemolyticus. J. Bacteriol. 177:1595-1609.
27. McCarter, L. L. 2001. Polar flagellar motility of the Vibrionaceae. Microbiol. Mol. Biol. Rev. 65:445-462.
28. McGee, K., P. Horstedt, and D. L. Milton. 1996. Identification and characterization of additional flagellin genes from Vibrio anguillarum. J. Bacteriol. 178:5188-5198.
29. Millikan, D. S., and E. G. Ruby. 2002. Alterations in Vibrio fischeri motility correlate with a delay in symbiosis initiation and are associated with additional symbiotic colonization defects. Appl. Environ. Microbiol. 68:2519-2528.
30. 54 transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J. Bacteriol. 185:3547-3557.
31. Milton, D. L., R. O'Toole, P. Hoerstedt, and H. Wolf-Watz. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
32. Nyholm, S. V., B. Deplancke, H. R. Gaskins, M. A. Apicella, and M. J. McFall-Ngai. 2002. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl. Environ. Microbiol. 68:5113-5122.
33. Nyholm, S. V., and M. J. McFall-Ngai. 2003. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl. Environ. Microbiol. 69:3932-3937.
34. Nyholm, S. V., E. V. Stabb, E. G. Ruby, and M. J. McFall-Ngai. 2000. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl. Acad. Sci. USA 97:10231-10235.
35. Pleier, E., and R. Schmitt. 1989. Identification and sequence analysis of two related flagellin genes in Rhizobium meliloti. J. Bacteriol. 171:1467-1475.
36. 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
37. Reichelt, J. L., and P. Baumann. 1973. Taxonomy of the marine, luminous bacteria. Arch. Mikrobiol. 94:283-330.
38. Ruby, E. G., and L. M. Asato. 1993. Growth and flagellation of vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch. Microbiol. 159:160-167.
39. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
40. Scharf, B., H. Schuster-Wolff-Buhring, R. Rachel, and R. Schmitt. 2001. Mutation analysis of the Rhizobium lupini H13-3 and Sinorhizobium meliloti flagellin genes: importance of flagellin A for flagellar filament structure and transcriptional regulation. J. Bacteriol. 183:5334-5342.
41. Silverman, M., J. Zieg, M. Hilmen, and M. Simon. 1979. Phase variation in Salmonella: genetic analysis of a recombinational switch. Proc. Natl. Acad. Sci. USA 76:391-395.
42. Stabb, E., K. Visick, D. S. Millikan, A. A. Corcoran, L. Gilson, S. V. Nyholm, M. McFall-Ngai, and E. Ruby. 2001. The Vibrio fischeri-Euprymna scolopes symbiosis: a model marine animal-bacteria interaction, p. 269-277. In Recent advances in marine science and technology. Pacon International, Honolulu, Hawaii.
43. +-glycohydrolases. J. Bacteriol. 183:309-317.
44. Stabb, E. V., and E. G. Ruby. 2003. New RP4-based plasmids for conjugation between Escherichia coli and members of the Vibrionaceae. Methods Enzymol. 358:413-426.
45. Swofford, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland, Mass.
46. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
47. Visick, K. L., and E. G. Ruby. 1997. New genetic tools for use in the marine bioluminescent bacterium Vibro fischeri, p. 119-122. In Bioluminescence and chemiluminescence. John Wiley and Sons, Chichester, United Kingdom.
48. Visick, K. L., and L. M. Skoufos. 2001. Two-component sensor required for normal symbiotic colonization of Euprymna scolopes by Vibrio fischeri. J. Bacteriol. 183:835-842.
49. 54 controls motility, biofilm formation, luminescence, and colonization. Appl. Environ. Microbiol. 70:2520-2524.
50. Young, G. M., M. J. Smith, S. A. Minnich, and V. L. Miller. 1999. The Yersinia enterocolitica motility master regulatory operon, flhDC, is required for flagellin production, swimming motility, and swarming motility. J. Bacteriol. 181:2823-2833.