The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae

Journal of Bacteriology

Volumn 189, Issue 6, 2007, Pages 2319-2330

  Fong, Jiunn C N ^a   Yildiz, Fitnat H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBOHYDRATE; EXOPOLYSACCHARIDE; GENE PRODUCT; HYDROLASE; MUTANT PROTEIN; PROTEIN BAP1; RUGOSE; SPACER DNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM COLONY; BACTERIUM MUTANT; BAP1 GENE; BIOFILM; CELL AGGREGATION; CONTROLLED STUDY; DELETION MUTANT; ENVIRONMENTAL STRESS; GENE CLUSTER; GENE DELETION; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; RBMB GENE; RBMBCDEF GENE; RBMC GENE; RBMD GENE; RBME GENE; RBMF GENE; SEQUENCE HOMOLOGY; VIBRIO CHOLERAE; VPS I GENE; VPS II GENE;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CULTURE MEDIA; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MULTIGENE FAMILY; PHENOTYPE; VIBRIO CHOLERAE;

VIBRIO CHOLERAE;

EID: 33947122068     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01569-06     Document Type: Article

References (71)

1. Albrecht, M. T., and N. L. Schiller. 2005. Alginate lyase (AlgL) activity is required for alginate biosynthesis in Pseudomonas aeruginosa. J. Bacteriol. 187:3869-3872.
2. Ali, A., Z. H. Mahmud, J. G. Morris, Jr., S. Sozhamannan, and J. A. Johnson. 2000. Sequence analysis of TnphoA insertion sites in Vibrio cholerae mutants defective in rugose polysaccharide production. Infect. Immun. 68: 6857-6864.
3. Ali, A., J. G. Morris, Jr., and J. A. Johnson. 2005. Sugars inhibit expression of the rugose phenotype of Vibrio cholerae. J. Clin. Microbiol. 43:1426-1429.
4. Allison, D. G., B. Ruiz, C. SanJose, A. Jaspe, and P. Gilbert. 1998. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167:179-184.
5. 1 that retains ligand recognition. J. Biol. Chem. 275: 5888-5903.
6. Bao, Y., D. P. Lies, H. Fu, and G. P. Roberts. 1991. An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of gram-negative bacteria. Gene 109:167-168.
7. Barbeyron, T., G. Michel, P. Potin, B. Henrissat, and B. Kloareg. 2000. ι-Carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of κ-carrageenases. J. Biol. Chem. 275:35499- 35505.
8. Bengoechea, J. A., E. Pinta, T. Salminen, C. Oertelt, O. Holst, J. Radziejewska-Lebrecht, Z. Piotrowska-Seget, R. Venho, and M. Skurnik. 2002. Functional characterization of Gne (UDP-N-acetylglucosamine-4-epimerase), Wzz (chain length determinant), and Wzy (O-antigen polymerase) of Yersinia enterocolitica serotype O:8. J. Bacteriol. 184:4277-4287.
9. Beyhan, S., A. D. Tischler, A. Camilli, and F. H. Yildiz. 2006. Differences in gene expression between the classical and El Tor biotypes of Vibrio cholerae O1. Infect. Immun. 74:3633-3642.
10. Bollag, D. M., M. D. Rozycki, and S. J. Edelstein. 1996. Protein methods, 2nd ed., p. 84-85. Eiley-Lis, Inc., New York, N.Y.
11. Boyd, A., and A. M. Chakrabarty. 1994. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 60:2355-2359.
12. Boyd, A., M. Ghosh, T. B. May, D. Shinabarger, R. Keogh, and A. M. Chakrabarty. 1993. Sequence of the algL gene of Pseudomonas aeruginosa and purification of its alginate lyase product. Gene 131:1-8.
13. Casper-Lindley, C., and F. H. Yildiz. 2004. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 186:1574-1578.
14. Chiavelli, D. A., J. W. Marsh, and R. K. Taylor. 2001. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67:3220-3225.
15. Costerton, J. W., Z. Lewandowski, D. E. Caldwell, D. R. Korber, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745.
16. de Lorenzo, V., and K. N. Timmis. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
17. Dow, J. M., L. Crossman, K. Findlay, Y. Q. He, J. X. Feng, and J. L. Tang. 2003. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc. Natl. Acad. Sci. USA 100:10995-11000.
18. Enos-Berlage, J. L., and L. L. McCarter. 2000. Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J. Bacteriol. 182:5513- 5520.
19. Faruque, S. M., M. J. Albert, and J. J. Mekalanos. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol. Mol. Biol. Rev. 62:1301-1314.
20. Fong, J. C., K. Karplus, G. K. Schoolnik, and F. H. Yildiz. 2006. Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae. J. Bacteriol. 188:1049-1059.
21. Fullner, K. J., and J. J. Mekalanos. 1999. Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect. Immun. 67:1393-1404.
22. Gjermansen, M., P. Ragas, C. Sternberg, S. Molin, and T. Tolker-Nielsen. 2005. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ. Microbiol. 7:894-906.
23. Han, F., Q. H. Gong, K. Song, J. B. Li, and W. G. Yu. 2004. Cloning, sequence analysis and expression of gene alyVI encoding alginate lyase from marine bacterium Vibrio sp. QY101. DNA Seq. 15:344-350.
24. Hatch, R. A., and N. L. Schiller. 1998. Alginate lyase promotes diffusion of aminoglycosides through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 42:974-977.
25. Henrissat, B., S. E. Heffron, M. D. Yoder, S. E. Lietzke, and F. Jurnak. 1995. Functional implications of structure-based sequence alignment of proteins in the extracellular pectate lyase superfamily. Plant Physiol. 107:963-976.
26. Herrero, M., V. de Lorenzo, and K. N. Timmis. 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.
27. Heydorn, A., A. T. Nielsen, M. Hentzer, C. Sternberg, M. Givskov, B. K. Ersboll, and S. Molin. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395-2407.
28. Horton, R. M. 1997. In vitro recombination and mutagenesis of DNA. SOEing together tailor-made genes. Methods Mol. Biol. 67:141-149.
29. Horton, R. M., S. N. Ho, J. K. Pullen, H. D. Hunt, Z. Cai, and L. R. Pease. 1993. Gene splicing by overlap extension. Methods Enzymol. 217:270-279.
30. Hung, D. T., J. Zhu, D. Sturtevant, and J. J. Mekalanos. 2006. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol. Microbiol. 59:193-201.
31. Jain, S., and D. E. Ohman. 2005. Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect. Immun. 73:6429-6436.
32. Jenkins, J., O. Mayans, and R. Pickersgill. 1998. Structure and evolution of parallel β-helix proteins. J. Struct. Biol. 122:236-246.
33. Jenkins, J., and R. Pickersgill. 2001. The architecture of parallel β-helices and related folds. Prog. Biophys. Mol. Biol. 77:111-175.
34. Kaper, J. B., J. G. Morris, Jr., and M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8:48-86.
35. Kaplan, J. B., C. Ragunath, N. Ramasubbu, and D. H. Fine. 2003. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous β-hexosaminidase activity. J. Bacteriol. 185:4693-4698.
36. Karplus, K., R. Karchin, C. Barrett, S. Tu, M. Cline, M. Diekhans, L. Grate, J. Casper, and R. Hughey. 2001. What is the value added by human intervention in protein structure prediction? Proteins Struct. Funct. Genet. 45: 86-91.
37. Karplus, K., S. Katzman, G. Shackleford, M. Koeva, J. Draper, B. Barnes, M. Soriano, and R. Hughey. 2005. SAM-T04: what's new in protein-structure prediction for CASP6. Proteins Struct. Funct. Bioinformat. 61:135-142.
38. Kawamoto, H., A. Horibe, Y. Mild, T. Kimura, K. Tanaka, T. Nakagawa, M. Kawamukai, and H. Matsuda. 2006. Cloning and sequencing analysis of alginate lyase genes from the marine bacterium Vibrio sp. O2. Mar. Biotechnol. 8:481-490.
39. Kelley, J. T., and C. D. Parker. 1981. Identification and preliminary characterization of Vibrio cholerae outer membrane proteins. J. Bacteriol. 145: 1018-1024.
40. Kitamikado, M., C. H. Tseng, K. Yamaguchi, and T. Nakamura. 1992. Two types of bacterial alginate lyases. Appl. Environ. Microbiol. 58:2474-2478.
41. Lefebvre, B., P. Formstecher, and P. Lefebvre. 1995. Improvement of the gene splicing overlap (SOE) method. BioTechniques 19:186-188.
42. Lim, B., S. Beyhan, J. Meir, and F. H. Yildiz. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60:331-348.
43. Loftus, J. C., J. W. Smith, and M. H. Ginsberg. 1994. Integrin-mediated cell adhesion: the extracellular face. J. Biol. Chem. 269:25235-25238.
44. Meibom, K. L., X. B. Li, A. T. Nielsen, C. Y. Wu, S. Roseman, and G. K. Schoolnik. 2004. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 101:2524-2529.
45. Michel, G., W. Helbert, R. Kahn, O. Dideberg, and B. Kloareg. 2003. The structural bases of the processive degradation of ι-carrageenan, a main cell wall polysaccharide of red algae. J. Mol. Biol. 334:421-433.
46. Miller, J. H. 1972. Assay of β-galactosidase, p. 352-355. In J. H. Miller (ed.), Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
47. 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.
48. 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.
49. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
50. Ott, C. M., D. F. Day, D. W. Koenig, and D. L. Pierson. 2001. The release of alginate lyase from growing Pseudomonas syringae pathovar phaseolicola. Curr. Microbiol. 42:78-81.
51. Parsek, M. R., and P. K. Singh. 2003. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701.
52. Petersen, T. N., S. Kauppinen, and S. Larsen. 1997. The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel beta helix. Structure 5:533-S44.
53. Reguera, G., and R. Kolter. 2005. Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J. Bacteriol. 187:3551-3555.
54. Rice, E. W., C. H. Johnson, R. M. Clark, K. R. Fox, J. D. 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 resist killing by chlorine, yet retains virulence. Int. J. Environ. Health Res. 3:89-98.
55. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.
56. Sauer, K., M. C. Cullen, A. H. Rickard, L. A. Zeef, D. G. Davies, and P. Gilbert. 2004. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J. Bacteriol. 186:7312-7326.
57. Schiller, N. L., S. R. Monday, C. M. Boyd, N. T. Keen, and D. E. Ohman. 1993. Characterization of the Pseudomonas aeruginosa alginate lyase gene (algL): cloning, sequencing, and expression in Escherichia coli. J. Bacteriol. 175:4780-4789.
58. Sugimura, I. I., T. Sawabe, and Y. Ezura. 2000. Cloning and sequence analysis of Vibrio halioticoli genes encoding three types of polyguluronate lyase. Mar. Biotechnol. 2:65-73.
59. Thormann, K. M., R. M. Saville, S. Shukla, and A. M. Spormann. 2005. Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J. Bacteriol. 187:1014-1021.
60. 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.
61. Wang, Y. H., G. L. Yu, X. M. Wang, Z. H. Lv, X. Zhao, Z. H. Wu, and W. S. Ji. 2006. Purification and characterization of alginate lyase from marine Vibrio sp. YWA. Acta Biochim. Biophys. Sin. 38:633-638.
62. 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.
63. Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586-595.
64. White, P. B. 1938. The rugose variant of vibrios. J. Pathol. 46:1-6.
65. Wong, T. Y., L. A. Preston, and N. L. Schiller. 2000. Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu. Rev. Microbiol. 54:289-340.
66. Xiong, J. P., T. Stehle, B. Diefenbach, R. Zhang, R. Dunker, D. L. Scott, A. Joachimiak, S. L. Goodman, and M. A. Arnaout. 2001. Crystal structure of the extracellular segment of integrin aVβ3. Science 294:339-345.
67. Xun, L. Y., R. A. Mah, and D. R. Boone. 1990. Isolation and characterization of disaggregatase from Methanosarcina mazei LYC. Appl. Environ. Microbiol. 56:3693-3698.
68. Yano, S., M. Wakayama, and T. Tachiki. 2006. Cloning and expression of an α-1,3-glucanase gene from Bacillus circulans KA-304: the enzyme participates in protoplast formation of Schizophyllum commune. Biosci. Biotechnol. Biochem. 70:1754-1763.
69. ETr-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183:1716-1726.
70. Yildiz, F. H., X. S. Liu, A. Heydorn, and G. K. Schoolnik. 2004. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 53:497-515.
71. 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.