A novel, conserved cluster of genes promotes symbiotic colonization and σ54-dependent biofilm formation by Vibrio fischeri

Molecular Microbiology

Volumn 57, Issue 5, 2005, Pages 1485-1498

  Yip, Emily S ^a   Grublesky, Brian T ^a   Hussa, Elizabeth A ^a   Visick, Karen L ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BETA GALACTOSIDASE; DNA; GLYCOSYLTRANSFERASE; OUTER MEMBRANE PROTEIN; RNA POLYMERASE;

ARTICLE; BACTERIAL COLONIZATION; BINDING SITE; BIOFILM; BIOSYNTHESIS; DNA SEQUENCE; ESCHERICHIA COLI; GENE; GENE CLUSTER; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; SYMBIOSIS; SYPA GENE; SYPG GENE; SYPI GENE; SYPM GENE; SYPP GENE; TRANSCRIPTION REGULATION; VIBRIO FISCHERI;

BACTERIAL PROTEINS; BASE SEQUENCE; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; SIGMA FACTOR; SYMBIOSIS; TRANSCRIPTION, GENETIC; VIBRIO FISCHERI;

CEPHALOPODA; EUPRYMNA SCOLOPES; VIBRIO FISCHERI; VIBRIO PARAHAEMOLYTICUS; VIBRIO VULNIFICUS;

EID: 23844545192     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04784.x     Document Type: Article

References (62)

1. Aeckersberg, F., Lupp, C., Feliciano, B., and Ruby, E.G. (2001) Vibrio fischeri outer membrane protein OmpU plays a role in normal symbiotic colonization. J Bacteriol 183: 6590-6597.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, DJ. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
4. Angelichio, M.J., and Camilli, A. (2002) In vivo expression technology. Infect Immun 70: 6518-6523.
5. Arrecubieta, C., Hammarton, T.C., Barrett, B., Chareonsudjai, S., Hodson, N., Rainey, D., and Roberts, I.S. (2001) The transport of group 2 capsular polysaccharides across the periplasmic space in Escherichia coli. Roles for the KpsE and KpsD proteins. J Biol Chem 276: 4245-4250.
6. Barrios, H., Valderrama, B., and Morett, E. (1999) Compilation and analysis of sigma(54)-dependent promoter sequences. Nucleic Acids Res 27: 4305-4313.
7. Bik, E.M., Bunschoten, A.E., Willems, R.J., Chang, A.C., and Mooi, F.R. (1996) Genetic organization and functional analysis of the otn DNA essential for cell-wall polysaccharide synthesis in Vibrio cholerae O139. Mol Microbiol 20: 799-811.
8. Boettcher, K.J., and Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172: 3701-3706.
9. Camilli, A., and Mekalanos, J.J. (1995) Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol Microbiol 18: 671-683.
10. Chen, C.Y., Wu, K.M., Chang, Y.C., Chang, C.H., Tsai, H.C., Liao, T.L., et al. (2003) Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13: 2577-2587.
11. Davidson, S.K., Koropatnick, T.A., Kossmehl, R., Sycuro, L., and McFall-Ngai, M.J. (2004) NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6: 1139-1151.
12. DeLoney, C.R., Bartley, T.M., and Visick, K.L. (2002) Role for phosphoglucomutase in Vibrio fischeri-Euprymna scolopes symbiosis. J Bacteriol 184: 5121-5129.
13. Djordjevic, D., Wiedmann, M., and McLandsborough, L.A. (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68: 2950-2958.
14. Dunn, A.K., Martin, M.O., and Stabb, E.V. (2005) Characterization of pES213, a small mobilization plasmid from Vibrio fischeri. Plasmid (in press).
15. Foster, J.S., and McFall-Ngai, M.J. (1998) Induction of apoptosis by cooperative bacteria in the morphogenesis of host epithelial tissues. Dev Genes Evol 208: 295-303.
16. Foster, J.S., Apicella, M.A., and McFall-Ngai, M.J. (2000) Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev Biol 226: 242-254.
17. Frideman, L., and Kolter, R. (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51: 675-690.
18. Graf, J., and Ruby, E.G. (1998) Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci USA 95: 1818-1822.
19. Graf, J., and Ruby, E.G. (2000) Novel effects of a transposon insertion in the Vibrio fischeri glnD gene: defects in iron uptake and symbiotic persistence in addition to nitrogen utilization. Mol Microbiol 37: 168-179.
20. Graf, J., Dunlap, P.V., and Ruby, E.G. (1994) Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J Bacteriol 176: 6986-6991.
21. Heidelberg, J.F., Eisen, J.A., Nelson, W.C., Clayton, R.A., Gwinn, M.L., Dodson, R.J., et al. (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477-483.
22. Herrero, M., DeLorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557-6567.
23. Jackson, K.D., Starkey, M., Kremer, S., Parsek, M.R., and Wozniak, D.J. (2004) Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186: 4466-4475.
24. Kikuchi, N., Kwon, Y.D., Gotoh, M., and Narimatsu, H. (2003) Comparison of glycosyltransferase families using the profile Hidden Markov Model. Biochem Biophys Res Comm 310: 574-579.
25. Kimbell, J.R., and McFall-Ngai, M.J. (2004) Symbiont-induced changes in host actin during the onset of a beneficial animal-bacterial association. Appl Environ Microbiol 70: 1434-1441.
26. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
27. Lupp, C., and Ruby, E.G. (2004) Vibrio fischeri LuxS and AinS: comparative study of two signal synthases. J Bacteriol 186: 3873-3881.
28. Lupp, C., and Ruby, E.G. (2005) Vibrio fischeri utilizes two quorum-sensing systems for the regulation of early and late colonization factors. J Bacteriol 187: 3620-3629.
29. Lupp, C., Urbanowski, M., Greenberg, E.P., and Ruby, E.G. (2003) The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol Microbiol 50: 319-331.
30. Makino, K., Oshima, K., Kurokawa, K., Yokoyama, K., Uda, T., Tagomori, K., et al. (2003) Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361: 743-749.
31. Marchler-Bauer, A., and Bryant, S.H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: W327-W331.
32. Matsukawa, M., and Greenberg, E.P. (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm. J Bacteriol 186: 4449-4456.
33. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
34. Millikan, D.S., and Ruby, E.G. (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.
35. Millikan, D.S., and Ruby, E.G. (2003) FlrA, a sigma54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J Bacteriol 185: 3547-3557.
36. Mishra, M., Parise, G., Jackson, K.D., Wozniak, D.J., and Deora, R. (2005) The BvgAS signal transduction system regulates biofilm development in Bordetella. J Bacteriol 187: 1474-1484.
37. Montgomery, M.K., and McFall-Ngai, M. (1993) Embryonic development of the light organ of the sepiolid squid Euprymna scolopes. Berry Biol Bull 184: 296-308.
38. Nesper, J., Hill, C., Paiment, A., Harauz, G., Beis, K., Naismith, J., and Whitfield, C. (2003) Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. J Biol Chem 278: 49763-49772.
39. Nyholm, S.V., and McFall-Ngai, M.J. (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.
40. Nyholm, S.V., and McFall-Ngai, M. (2004) The winnowing: establishing the squid- Vibrio symbiosis. Nat Rev Microbiol 2: 632-642.
41. Nyholm, S.V., Stabb, E.V., Ruby, E.G., and McFall-Ngai, M.J. (2000) Establishment of an animal-bacterial association: recruiting symbiotic Vibrios from the environment. Proc Natl Acad Sci USA 97: 10231-10235.
42. Parsek, M.R., and Singh, P.K. (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701.
43. Parsek, M.R., and Fuqua, C. (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. J Bacteriol 186: 4427-4440.
44. Reitzer, L., and Schneider, B.L. (2001) Metabolic context and possible physiological themes of sigma(54)-dependent genes in Escherichia coli. Microbiol Mol Biol Rev 65: 422-444.
45. Ruby, E.G. (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50: 591-624.
46. Ruby, E.G. (1999) The Euprymna scolopes-Vibrio fischeri symbiosis: a biomedical model for the study of bacterial colonization of animal tissue. J Mol Microbiol Biotechnol 1: 13-21.
47. Ruby, E.G., and Asato, L.M. (1993) Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 159: 160-167.
48. Ruby, E.G., and Nealson, K.H. (1977) Pyruvate production and excretion by the luminous marine bacteria. Appl Environ Microbiol 34: 164-169.
49. Ruby, E.G., Urbanowski, M., Campbell, J., Dunn, A., Faini, M., Gunsalus, R., et al. (2005) Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA 102: 3004-3009.
50. Stabb, E.V., and Ruby, E.G. (2002) New RP4-based plasmids for conjugation between Escherichia coli and members of the Vibrionaceae. Methods Enzymol 358:413-426.
51. Stabb, E.V., Butler, M.S., and Adin, D.M. (2004) Correlation between osmolarity and luminescence of symbiotic Vibrio fischeri strain ES114. J Bacteriol 186: 2906-2908.
52. Takeda, S., Fujisawa, Y., Matsubara, M., Aiba, H., and Mizuno, T. (2001) A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC → YojN → RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol Microbiol 40: 440-450.
53. Totten, P.A., and Lory, S. (1990) Characterization of the type a flagellin gene from Pseudomonas aeruginosa PAK. J Bacteriol 172: 7188-7199.
54. Upreti, R.K., Kumar, M., and Shankar, V. (2003) Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics 3: 363-379.
55. Visick, K.L., and Ruby, E.G. (1998) The periplasmic, group III catalase of Vibrio fischeri is required for normal symbiotic competence and is induced both by oxidative stress and by approach to stationary phase. J Bacteriol 180: 2087-2092.
56. Visick, K.L., and Skoufos, L.M. (2001) Two-component sensor required for normal symbiotic colonization of Euprymna scolopes by Vibrio fischeri. J Bacteriol 183: 835-842.
57. Visick, K.L., Foster, J., Doino, J., McFall-Ngai, M., and Ruby, E.G. (2000) Vibrio fischen lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182: 4578-4586.
58. Whistler, C.A., and Ruby, E.G. (2003) GacA regulates symbiotic colonization traits of Vibrio fischeri and facilitates a beneficial association with an animal host. J Bacteriol 185: 7202-7212.
59. 54 controls motility, biofilm formation, luminescence, and colonization. Appl Environ Microbiol 70: 2520-2524.
60. Woodcock, D.M., Crowther, P.J., Doherty, J., Jefferson, S., DeCruz, E., Noyer-Weidner, M., et al. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17: 3469-3478.
61. Yoon, S.S., Hennigan, G.M., Milliard, G.M., Ochsner, U.A., Parvatiyar, K., Kamani, M.C., et al. (2002) Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3: 593-603.
62. Zhang, Z., Kochhar, S., and Grigorov, M. (2003) Exploring the sequence-structure protein landscape in the glycosyltransferase family. Protein Sci 12: 2291-2302.