Role of capsular polysaccharide (CPS) in biofilm formation and regulation of CPS production by quorum-sensing in Vibrio vulnificus

Molecular Microbiology

Volumn 90, Issue 4, 2013, Pages 841-857

  Lee, Kyung Jo ^a   Kim, Jeong A ^a   Hwang, Won ^a,b   Park, Soon Jung ^b   Lee, Kyu Ho ^a  

^a Sogang University   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA N ACETYLGALACTOSAMINIDASE; BACTERIAL CAPSULAR POLYSACCHARIDE; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; PROTEIN SMCR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BIOFILM; CARBOHYDRATE SYNTHESIS; CELL AGGREGATION; CELL DENSITY; CONTROLLED STUDY; GENE CLUSTER; GENE INACTIVATION; GENETIC TRANSCRIPTION; HYDROPHOBICITY; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; QUORUM SENSING; VIBRIO VULNIFICUS; WBPP GENE; WILD TYPE;

VIBRIO VULNIFICUS;

ACETYLGLUCOSAMINIDASE; BACTERIAL CAPSULES; BACTERIAL PROTEINS; BIOFILMS; CARBOHYDRATE EPIMERASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; GENES, BACTERIAL; LIPOPOLYSACCHARIDES; MULTIGENE FAMILY; QUORUM SENSING; SIGNAL TRANSDUCTION; VIBRIO VULNIFICUS;

EID: 84887402410     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12401     Document Type: Article

References (62)

1. Balebona, M.C., Moriñigo, M.A., and Borrego, J.J. (2001) Hydrophobicity and adhesion to fish cells and mucus of Vibrio strains isolated from infected fish. Int Microbiol 4: 21-26.
2. Biosca, E.G., Oliver, J.D., and Amaro, C. (1996) Phenotypic characterization of Vibrio vulnificus biotype 2, a lipopolysaccharide-based homogeneous O serogroup within Vibrio vulnificus. Appl Environ Microbiol 62: 918-927.
3. Boles, B.R., and Horswill, A.R. (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4: e1000052.
4. Cantón, R., Ruiz-Garbajosa, P., Chaves, R.L., and Johnson, A.P. (2010) A potential role for daptomycin in enterococcal infections: what is the evidence? J Antimicrob Chemother 65: 1126-1136.
5. Cao, B., Shi, L., Brown, R.N., Xiong, Y., Fredrickson, J.K., Romine, M.F., etal. (2011) Extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms: characterization by infrared spectroscopy and proteomics. Environ Microbiol 13: 1018-1031.
6. Chatzidaki-Livanis, M., Jones, M.K., and Wright, A.C. (2006) Genetic variation in the Vibrio vulnificus group I capsular polysaccharide operon. J Bacteriol 188: 1987-1998.
7. Chen, C.-Y., Wu, K.-M., Chang, Y.-C., Chang, C.-H., Tsai, H.-C., Liao, T.-L., etal. (2003) Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13: 2577-2587.
8. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., and Lappin-Scott, H.M. (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
9. Creuzenet, C., Belanger, M., Wakarchuk, W.W., and Lam, J.S. (2000) Expression, purification, and biochemical characterization of WbpP, a new UDP-GlcNAc C4 epimerase from Pseudomonas aeruginosa serotype O6. J Biol Chem 275: 19060-19067.
10. Davies, D.G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W., and Greenberg, E.P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295-298.
11. De Kievit, T.R. (2009) Quorum sensing in Pseudomonas aeruginosa biofilms. Environ Microbiol 11: 279-288.
12. Donlan, R.M. (2001) Biofilms and device-associated infections. Emerg Infect Dis 7: 277-281.
13. Donlan, R.M., and Costerton, J.W. (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15: 167-193.
14. Eboigbodin, K.E., and Biggs, C.A. (2008) Characterization of the extracellular polymeric substances produced by Escherichia coli using infrared spectroscopic, proteomic, and aggregation studies. Biomacromolecules 9: 686-695.
15. Enos-Berlage, J.L., and McCarter, L.L. (2000) Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J Bacteriol 182: 5513-5520.
16. Flemming, H.C., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
17. Fuqua, W.C., Winans, S.C., and Greenberg, E.P. (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-275.
18. Grau, B.L., Henk, M.C., Garrison, K.L., Olivier, B.J., Schulz, R.M., O'Reilly, K.L., and Pettis, G.S. (2008) Further characterization of Vibrio vulnificus rugose exopolysaccharide gene cluster. Infect Immun 76: 1485-1497.
19. Greenberg, E.P., Hastings, J.W., and Ulitzer, S. (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120: 87-91.
20. Gulig, P.A., Bourdage, K.L., and Starks, A.M. (2005) Molecular pathogenesis of Vibrio vulnificus. J Microbiol 43: 118-131.
21. Hammer, B.K., and Bassler, B.L. (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50: 101-104.
22. Hayat, U., Reddy, G.P., Bush, C.A., Johnson, J.A., Wright, A.C., and Morris, J.G., Jr (1993) Capsular types of Vibrio vulnificus: an analysis of strains from clinical and environmental sources. J Infect Dis 168: 758-762.
23. Jacques, M. (1996) Role of lipo-oligosaccharides and lipopolysccharides in bacterial adherence. Trends Microbiol 4: 408-410.
24. Jeong, H.S., Jeong, K.C., Choi, H.K., Park, K.-J., Lee, K.-H., Rhee, J.H., and Choi, S.H. (2001) Differential expression of Vibrio vulnificus elastase gene in a growth phase-dependent manner by two different types of promoters. J Biol Chem 276: 13875-13880.
25. Jeong, H.S., Lee, M.H., Lee, K.-H., Park, S.-J., and Choi, S.H. (2003) SmcR and cyclic AMP receptor protein coactivate Vibrio vulnificus vvpE encoding elastase through the RpoS-dependent promoter in a synergistic manner. J Biol Chem 278: 45072-45081.
26. Jiang, P., Li, J., Han, F., Duan, G., Lu, X., Gu, Y., and Yu, W. (2011) Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS ONE 6: e18514.
27. Joseph, L.A., and Wright, A.C. (2004) Expression of Vibrio vulnificus capsular polysaccharide inhibits biofilm formation. J Bacteriol 186: 889-893.
28. Kaplan, J.B. (2010) Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 89: 205-218.
29. Karatan, E., and Watnick, P. (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73: 310-347.
30. Keen, N.T., Tamaki, S., Kobayashi, D., and Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70: 191-197.
31. Kim, H.-S., Lee, M.-A., Chun, S.-J., Park, S.-J., and Lee, K.-H. (2007) Role of NtrC in biofilm formation via controlling expression of the gene encoding an ADP-glycero-manno-heptose-6-epimerase in the pathogenic bacterium, Vibrio vulnificus. Mol Microbiol 63: 559-574.
32. Kim, H.-S., Park, S.-J., and Lee, K.-H. (2009) Role of NtrC-regulated exopolysaccharides in the biofilm formation and pathogenic interaction of Vibrio vulnificus. Mol Microbiol 74: 436-453.
33. Kim, S.Y., Lee, S.E., Kim, Y.R., Kim, C.M., Ryu, P.Y., Choy, H.E., etal. (2003a) Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol Microbiol 48: 1647-1664.
34. Kim, Y.R., Lee, S.E., Kim, C.M., Kim, S.Y., Shin, E.K., Shin, D.H., etal. (2003b) Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 71: 5461-5471.
35. Lee, D.H., Jeong, H.S., Jeong, H.G., Kim, K.M., Kim, H., and Choi, S.H. (2008) A consensus sequence for binding of SmcR, a Vibrio vulnificus LuxR homologue, and genome-wide identification of the SmcR regulon. J Biol Chem 283: 23610-23618.
36. Lee, J.-H., Rho, J.B., Park, K.-J., Kim, C.B., Han, Y.-S., Choi, S.H., etal. (2004) Role of Flagellum and motility in pathogenesis of Vibrio vulnificus. Infect Immun 72: 4905-4910.
37. Lenz, D.H., Mok, K.C., Lilley, B.N., Kulkarni, R.V., Wingreen, N.S., and Bassler, B.L. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
38. Lewis, K. (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5: 48-56.
39. McDougald, D., Lin, W.H., Rice, S.A., and Kjelleberg, S. (2006) The role of quorum sensing and the effect of environmental conditions on biofilm formation by strains of Vibrio vulnificus. Biofouling 22: 161-172.
40. Ng, W.L., and Bassler, B.L. (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
41. O'Toole, G.A., and Kolter, R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol Microbiol 28: 449-461.
42. Park, J.H., Cho, Y.-J., Chun, J., Seok, Y.-J., Lee, J.K., Kim, K.-S., etal. (2011) Complete genome sequence of Vibrio vulnificus MO6-24/O. J Bacteriol 193: 2062-2063.
43. Park, N.-Y., Lee, J.-H., Kim, M.-W., Jeong, H.-G., Lee, B.-C., Kim, T.-S., etal. (2006) Identification of the Vibrio vulnificus wbpP gene and evaluation of its role in virulence. Infect Immun 74: 721-728.
44. Parsek, M.R., and Singh, P.K. (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701.
45. Pompilio, A., Piccolomini, R., Picciani, C., D'Antonio, D., Savini, V., and Di Bonaventura, G. (2008) Factors associated with adherence to and biofilm formation on polystyrene by Stenotrophomonas maltophilia: the role of cell surface hydrophobicity and motility. FEMS Microbiol Lett 287: 41-47.
46. Powell, J.L., Wright, A.C., Wasserman, S.S., Hone, D.M., and Morris, J.G. Jr (1997) Release of tumor necrosis factor alpha in response to Vibrio vulnificus capsular polysaccharide in in vivo and in vitro models. Infect Immun 65: 3713-3718.
47. Reddy, G.P., Hayat, U., Abeygunawardana, C., Fox, C., Wright, A.C., Maneval, D.R. Jr, etal. (1992) Purification and determination of the structure of capsular polysaccharide of Vibrio vulnificus MO6-24. J Bacteriol 174: 2620-2630.
48. Roh, J.-B., Lee, M.-A., Lee, H.-J., Kim, S.-M., Cho, Y., Kim, Y.-J., etal. (2006) Transcriptional regulatory cascade for elastase production in Vibrio vulnificus: LuxO activates luxT expression and LuxT represses smcR expression. J Biol Chem 281: 34775-34784.
49. Sakuragi, Y., and Kolter, R. (2007) Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol 189: 5383-5386.
50. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
51. Sayem, S.M., Manzo, E., Ciavatta, L., Tramice, A., Cordone, A., Zanfardino, A., etal. (2011) Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microb Cell Fact 10: 74.
52. Schaber, J.A., Triffo, W.J., Suh, S.J., Oliver, J.W., Hastert, M.C., Griswold, J.A., etal. (2007) Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect Immun 75: 3715-3721.
53. Simon, R., Priefer, U., and Pülher, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Nat Biotechnol 1: 784-791.
54. Stepanović, S., Cirković, I., Ranin, L., and Svabić-Vlahović, M. (2004) Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 38: 428-432.
55. Strom, M.S., and Paranjpye, R.N. (2000) Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect 2: 177-188.
56. Taylor, K.A.C.C. (1993) A colorimetric method for the quantitation of galacturonic acid. Appl Biochem Biotechnol 43: 51-54.
57. Valle, J., Da Re, S., Henry, N., Fontaine, T., Balestrino, D., Latour-Lambert, P., and Ghigo, J.M. (2006) Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci USA 103: 12558-12563.
58. Whitfield, C. (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.
59. Wright, A.C., Simpson, L.M., Oliver, J.D., and Morris, J.G., Jr (1990) Phenotypic evaluation of acapsular transposon mutants of Vibrio vulnificus. Infect Immun 58: 1769-1773.
60. Wright, A.C., Powell, J.L., Tanner, M.K., Ensor, L.A., Karpas, A.B., Morris, J.G., Jr, and Sztein, M.B. (1999) Differential expression of Vibrio vulnificus capsular polysaccharide. Infect Immun 67: 2250-2257.
61. Yildiz, F.H., and Visick, K.L. (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17: 109-118.
62. Zhu, J., and Mekalanos, J.J. (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5: 647-656.