Expression of the primary carbohydrate component of the Bordetella bronchiseptica biofilm matrix is dependent on growth phase but independent of Bvg regulation

Journal of Bacteriology

Volumn 188, Issue 18, 2006, Pages 6680-6687

  Irie, Yasuhiko ^a   Preston, Andrew ^b   Yuk, Ming H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CARBOHYDRATE; DOUBLE STRANDED DNA; GREEN FLUORESCENT PROTEIN; HEMAGGLUTININ; HEMOLYSIN; LECTIN; N ACETYLGLUCOSAMINE; VIRULENCE FACTOR; WHEAT GERM AGGLUTININ; XYLOSE; YELLOW FLUORESCENT PROTEIN;

ARTICLE; ASSAY; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIOASSAY; BIOFILM; BORDETELLA BRONCHISEPTICA; BVGAS GENE; ENZYME LINKED LECTIN SORBENT ASSAY; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; GAS CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PLASMID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACETYLGLUCOSAMINE; BACTERIAL PROTEINS; BIOFILMS; BORDETELLA; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; POLYSACCHARIDES, BACTERIAL; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; XYLOSE;

BACTERIA (MICROORGANISMS); BORDETELLA BRONCHISEPTICA;

EID: 33748873117     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00605-06     Document Type: Article

References (48)

1. 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.
2. Bar-Peled, M., C. L. Griffith, and T. L. Doering. 2001. Functional cloning and characterization of a UDP-glucuronic acid decarboxylase: the pathogenic fungus Cryptococcus neoformans elucidates UDP-xylose synthesis. Proc. Natl. Acad. Sci. USA 98:12003-12008.
3. Branda, S. S., S. Vik, L. Friedman, and R. Kolter. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13:20-26.
4. Cotter, P. A., and A. M. Jones. 2003. Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol. 11:367-373.
5. Cotter, P. A., and J. F. Miller. 1994. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect. Immun. 62:3381-3390.
6. Cotter, P. A., and J. F. Miller. 1997. A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol. Microbiol. 24:671-685.
7. Cummings, C. A., H. J. Bootsma, D. A. Relman, and J. F. Miller. 2006. Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J. Bacteriol. 188:1775-1785.
8. Davies, D. 2003. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2:114-122.
9. Deretic, V., J. R. Govan, W. M. Konyecsni, and D. W. Martin. 1990. Mucoid Pseudomonas aeruginosa in cystic fibrosis: mutations in the muc loci affect transcription of the algR and algD genes in response to environmental stimuli. Mol. Microbiol. 4:189-196.
10. Friedman, L., and R. Kolter. 2004. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186:4457-4465.
11. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95-108.
12. Harper, A. D., and M. Bar-Peled. 2002. Biosynthesis of UDP-xylose. Cloning and characterization of a novel Arabidopsis gene family, UXS, encoding soluble and putative membrane-bound UDP-glucuronic acid decarboxylase isoforms. Plant Physiol. 130:2188-2198.
13. Harrill, E. T., P. A. Cotter, M. H. Yuk, and J. F. Miller. 1999. Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect. Immun. 67:1493-1500.
14. Hsu, K. L., K. T. Pilobello, and L. K. Mahal. 2006. Analyzing the dynamic bacterial glycome with a lectin microarray approach. Nat. Chem. Biol. 2:153-157.
15. Irie, Y., S. Mattoo, and M. H. Yuk. 2004. The Bvg virulence control system regulates biofilm formation in Bordetella bronchiseptica. J. Bacteriol. 186:5692-5698.
16. Irie, Y., G. A. O'Toole, and M. H. Yuk. 2005. Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol. Lett. 250:237-243.
17. Jackson, K. D., M. Starkey, S. Kremer, M. R. Parsek, and D. J. Wozniak. 2004. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol. 186:4466-4475.
18. Kaplan, J. B., C. Ragunath, N. Ramasubbu, and D. H. Fine. 2003. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J. Bacteriol. 185:4693-4698.
19. Kaplan, J. B., K. Velliyagounder, C. Ragunath, H. Rohde, D. Mack, J. K. Knobloch, and N. Ramasubbu. 2004. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J. Bacteriol. 186:8213-8220.
20. Klausen, M., A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50:61-68.
21. Kuchma, S. L., J. P. Connolly, and G. A. O'Toole. 2005. A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J. Bacteriol. 187:1441-1454.
22. Lee, S. F., Y. H. Li, and G. H. Bowden. 1996. Detachment of Streptococcus mutans biofilm cells by an endogenous enzymatic activity. Infect. Immun. 64:1035-1038.
23. Leriche, V., P. Sibille, and B. Carpentier. 2000. Use of an enzyme-linked lectinsorbent assay to monitor the shift in polysaccharide composition in bacterial biofilms. Appl. Environ. Microbiol. 66:1851-1856.
24. Mack, D., W. Fischer, A. Krokotsch, K. Leopold, R. Hartmann, H. Egge, and R. Laufs. 1996. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178:175-183.
25. Maira-Litran, T., A. Kropec, C. Abeygunawardana, J. Joyce, G. Mark III, D. A. Goldmann, and G. B. Pier. 2002. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect. Immun. 70:4433-4440.
26. Matsukawa, M., and E. P. Greenberg. 2004. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186:4449-4456.
27. Merkle, R. K., and I. Poppe. 1994. Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry. Methods Enzymol. 230:1-15.
28. Miller, V. L., and J, J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
29. Mishra, M., G. Parise, K. D. Jackson, D. J. Wozniak, and R. Deora. 2005. The BvgAS signal transduction system regulates biofilm development in Bordetella. J. Bacteriol. 187:1474-1484.
30. Moorthy, S., and P. I. Watnick. 2004. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol. Microbiol. 52:573-587.
31. Moriarity, J. L., K. J. Hurt, A. C. Resnick, P. B. Storm, W. Laroy, R. L. Schnaar, and S. H. Snyder. 2002. UDP-glucuronate decarboxylase, a key enzyme in proteoglycan synthesis: cloning, characterization, and localization. J. Biol. Chem. 277:16968-16975.
32. Murphy, L. A., and I. J. Goldstein. 1977. Five α-D- galactopyranosyl-binding isolectins from Bandeiraea simplicifolia seeds. J. Biol. Chem. 252:4739-4742.
33. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
34. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
35. Parkhill, J., M. Sebaihia, A. Preston, L. D. Murphy, N. Thomson, D. E. Harris, M. T. Holden, C. M. Churcher, S. D. Bentley, K. L. Mungall, A. M. Cerdeño-Tárraga, L. Temple, K. James, B. Harris, M. A. Quail, M. Achtman, R. Atkin, S. Baker, D. Basham, N. Bason, I. Cherevach, T. Chillingworth, M. Collins, A. Cronín, P. Davis, J. Doggett, T. Feltwell, A. Goble, N. Hamlin, H. Hauser, S. Holroyd, K. Jagels, S. Leather, S. Moule, H. Norberczak, S. O'Neil, D. Ormond, C. Price, E. Rabbinowitsch, S. Rutter, M. Sanders, D. Saunders, K. Seeger, S. Sharp, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, L. Unwin, S. Whitehead, B. G. Barrell, and D. J. Maskell. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:32-40.
36. Preston, A., B. O. Petersen, J. Ø. Duus, J. Kubler-Kielb, G. Ben-Menachem, J. Li, and E. Vinogradov. 2006. Complete structures of Bordetella bronchiseptica and Bordetella parapertussis lipopolysaccharides. J. Biol. Chem. 281:18135-18144.
37. Stainer, D. W., and M. J. Scholte. 1970. A simple chemically defined medium for the production of phase I Bordetella pertussis. J. Gen. Microbiol. 63:211-220.
38. Stockbauer, K. E., B. Fuchslocher, J. F, Miller, and P. A. Cotter, 2001. Identification and characterization of BipA, a Bordetella Bvg-intermediate phase protein. Mol. Microbiol. 39:65-78.
39. Strathmann, M., J. Wingender, and H. C. Flemming. 2002. Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. J. Microbiol. Methods 50:237-248.
40. Sutherland, I. W. 2001. The biofilm matrix-an immobilized but dynamic microbial environment. Trends Microbiol. 9:222-227.
41. Wang, X., J. F. Preston III, and T. Romeo. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186:2724-2734.
42. Webb, J. S., M, Givskov, and S. Kjelleberg. 2003. Bacterial biofilms: prokaryotic adventures in multicellularity. Curr. Opin. Microbiol. 6:578-585.
43. Whitchurch, C. B., T. Tolker-Nielsen, P. C. Ragas, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487.
44. Williams, C. L., P. E. Boucher, S. Stibitz, and P. A. Cotter. 2005. BvgA functions as both an activator and a repressor to control Bvg phase expression of bipA in Bordetella pertussis. Mol. Microbiol. 56:175-188,
45. Wingender, J., M. Strathmann, A. Rode, A. Leis, and H. C. Flemming. 2001. Isolation and biochemical characterization of extracellular polymeric substances from Pseudomonas aeruginosa. Methods Enzymol. 336:302-314.
46. Wozniak, D. J., T. J. Wyckoff, M. Starkey, R. Keyser, P. Azadi, G. A. O'Toole, and M. R. Parsek. 2003. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc. Natl. Acad. Sci. USA 100:7907-7912.
47. York, W. S., A. G. Darvill, M. McNeil, T. T. Stevenson, and P. Albersheim. 1986. Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol. 118:3-40.
48. Zogaj, X., M. Nimtz, M. Rohde, W. Bokranz, and U. Römling. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:1452-1463.