Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix

Molecular Microbiology

Volumn 75, Issue 4, 2010, Pages 827-842

  Borlee, Bradley R ^a   Goldman, Aaron D ^a   Murakami, Keiji ^a   Samudrala, Ram ^a   Wozniak, Daniel J ^b   Parsek, Matthew R ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CYCLIC GMP; LECTIN; MANNOSE; POLYSACCHARIDE;

ARTICLE; BACTERIAL GENE; BIOFILM; BIOMASS; CDRA GENE; EXTRACELLULAR MATRIX; GENE EXPRESSION; LIQUID CULTURE; MUTATION; NONHUMAN; OPERON; OUTER MEMBRANE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; SECOND MESSENGER; SUPERNATANT; WESTERN BLOTTING;

ADHESINS, BACTERIAL; BIOFILMS; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MUTATION; OPERON; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 76449122382     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06991.x     Document Type: Article

References (70)

1. Bendtsen, J.D., Nielsen, H., von Heijne, G. Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 : 783 795.
2. Bennett-Lovsey, R.M., Herbert, A.D., Sternberg, M.J. Kelley, L.A. (2008) Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70 : 611 625.
3. van den Berg, B.M., Beekhuizen, H., Willems, R.J., Mooi, F.R. van Furth, R. (1999) Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect Immun 67 : 1056 1062.
4. Boles, B.R., Thoendel, M. Singh, P.K. (2004) Self-generated diversity produces 'insurance effects' in biofilm communities. Proc Natl Acad Sci USA 101 : 16630 16635.
5. Bryson, K., McGuffin, L.J., Marsden, R.L., Ward, J.J., Sodhi, J.S. Jones, D.T. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res 33 : W36 W38.
6. Byrd, M.S., Sadovskaya, I., Vinogradov, E., Lu, H., Sprinkle, A.B., Richardson, S.H., et al. (2009) Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol Microbiol 73 : 622 638.
7. Canutescu, A.A., Shelenkov, A.A. Dunbrack, R.L., Jr. (2003) A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci 12 : 2001 2014.
8. Chevalier, N., Moser, M., Koch, H.G., Schimz, K.L., Willery, E., Locht, C., et al. (2004) Membrane targeting of a bacterial virulence factor harbouring an extended signal peptide. J Mol Microbiol Biotechnol 8 : 7 18.
9. Croft, L., Beatson, S.A., Whitchurch, C.B., Huang, B., Blakeley, R.L. Mattick, J.S. (2000) An interactive web-based Pseudomonas aeruginosa genome database: discovery of new genes, pathways and structures. Microbiology 146 Pt 10 2351 2364.
10. Danese, P.N., Pratt, L.A., Dove, S.L. Kolter, R. (2000) The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol 37 : 424 432.
11. Davies, D.G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W., Greenberg, E.P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280 : 295 298.
12. D'Argenio, D.A., Calfee, M.W., Rainey, P.B. Pesci, E.C. (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184 : 6481 6489.
13. Drenkard, E. Ausubel, F.M. (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416 : 740 743.
14. Eagon, R.G. (1962) Composition of an extracellular slime produced by Pseudomonas aeruginosa. Can J Microbiol 8 : 585.
15. Friedman, L. Kolter, R. (2004a) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51 : 675 690.
16. Friedman, L. Kolter, R. (2004b) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186 : 4457 4465.
17. Gjermansen, M., Ragas, P. Tolker-Nielsen, T. (2006) Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett 265 : 215 224.
18. Guvener, Z.T. Harwood, C.S. (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66 : 1459 1473.
19. Hasman, H., Chakraborty, T. Klemm, P. (1999) Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181 : 4834 4841.
20. Haussler, S., Tummler, B., Weissbrodt, H., Rohde, M. Steinmetz, I. (1999) Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29 : 621 625.
21. Henderson, I.R., Meehan, M. Owen, P. (1997) Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol Lett 149 : 115 120.
22. Hentzer, M., Teitzel, G.M., Balzer, G.J., Heydorn, A., Molin, S., Givskov, M. Parsek, M.R. (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183 : 5395 5401.
23. Hickman, J.W. Harwood, C.S. (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69 : 376 389.
24. Hickman, J.W., Tifrea, D.F. Harwood, C.S. (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102 : 14422 14427.
25. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212 : 77 86.
26. Holloway, B.W. (1995) Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13 : 572 581.
27. Hsu, F, Schwarz, S. Mougous, J.D. (2009) TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol Microbiol 72 : 1111 1125.
28. Jackson, K.D., Starkey, M., Kremer, S., Parsek, M.R. 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.
29. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292 : 195 202.
30. Kabsch, W. Sander, C. (1983) How good are predictions of protein secondary structure? FEBS Lett 155 : 179 182.
31. Kajava, A.V., Cheng, N., Cleaver, R., Kessel, M., Simon, M.N., Willery, E., et al. (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42 : 279 292.
32. Kaneko, Y., Thoendel, M., Olakanmi, O., Britigan, B.E., Singh, P.K. (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117 : 877 888.
33. Kirisits, M.J., Prost, L., Starkey, M. Parsek, M.R. (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71 : 4809 4821.
34. Kjaergaard, K., Schembri, M.A., Ramos, C., Molin, S. Klemm, P. (2000) Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol 2 : 695 702.
35. Lequette, Y., Lee, J.H., Ledgham, F., Lazdunski, A. Greenberg, E.P. (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188 : 3365 3370.
36. Levitt, M., Hirshberg, M., Sharon, R. Daggett, V. (1995) Potential energy function and parameters for simulations of the molecular dynamics of proteins and nucleic acids in solution. Comput Phys Commun 91 : 215 231.
37. de Luna, M.G., Scott-Tucker, A., Desvaux, M., Ferguson, P., Morin, N.P., Dudley, E.G., et al. (2008) The Escherichia coli biofilm-promoting protein Antigen 43 does not contribute to intestinal colonization. FEMS Microbiol Lett 284 : 237 246.
38. Ma, L., Jackson, K.D., Landry, R.M., Parsek, M.R. Wozniak, D.J. (2006) Analysis of Pseudomonas aeruginosa conditional Psl variants reveals roles for the Psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188 : 8213 8221.
39. Ma, L., Lu, H., Sprinkle, A., Parsek, M.R. Wozniak, D.J. (2007) Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189 : 8353 8356.
40. Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K. Wozniak, D.J. (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5 : e1000354.
41. Marchler-Bauer, A., Anderson, J.B., Derbyshire, M.K., DeWeese-Scott, C., Gonzales, N.R., Gwadz, M., et al. (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35 : D237 D240.
42. Marsden, R.L., McGuffin, L.J. Jones, D.T. (2002) Rapid protein domain assignment from amino acid sequence using predicted secondary structure. Protein Sci 11 : 2814 2824.
43. Matsukawa, M. Greenberg, E.P. (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186 : 4449 4456.
44. Mazar, J. Cotter, P.A. (2007) New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15 : 508 515.
45. Menozzi, F.D., Boucher, P.E., Riveau, G., Gantiez, C. Locht, C. (1994a) Surface-associated filamentous hemagglutinin induces autoagglutination of Bordetella pertussis. Infect Immun 62 : 4261 4269. (Pubitemid 24301951)
46. Menozzi, F.D., Mutombo, R., Renauld, G., Gantiez, C., Hannah, J.H., Leininger, E., et al. (1994b) Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect Immun 62 : 769 778. (Pubitemid 24065554)
47. Mougous, J.D., Cuff, M.E., Raunser, S., Shen, A., Zhou, M., Gifford, C.A., et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 : 1526 1530.
48. Newman, J.R., Fuqua, C. (1999) Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227 : 197 203.
49. O'Toole, G.A. Kolter, R. (1998a) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30 : 295 304.
50. O'Toole, G.A. Kolter, R. (1998b) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28 : 449 461.
51. Rahme, L.G., Stevens, E.J., Wolfort, S.F., Shao, J., Tompkins, R.G. Ausubel, F.M. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268 : 1899 1902.
52. Rani, S.A., Pitts, B., Beyenal, H., Veluchamy, R.A., Lewandowski, Z., Davison, W.M., et al. (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189 : 4223 4233.
53. Relman, D., Tuomanen, E., Falkow, S., Golenbock, D.T., Saukkonen, K. Wright, S.D. (1990) Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61 : 1375 1382.
54. Samudrala, R. Moult, J. (1998) An all-atom distance-dependent conditional probability discriminatory function for protein structure prediction. J Mol Biol 275 : 895 916.
55. Schaefer, A.L., Greenberg, E.P. Parsek, M.R. (2001) Acylated homoserine lactone detection in Pseudomonas aeruginosa biofilms by radiolabel assay. Methods Enzymol 336 : 41 47.
56. Schembri, M.A., Dalsgaard, D. Klemm, P. (2004) Capsule shields the function of short bacterial adhesins. J Bacteriol 186 : 1249 1257.
57. Simm, R., Morr, M., Kader, A., Nimtz, M. Romling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53 : 1123 1134.
58. Smith, E.E., Buckley, D.G., Wu, Z., Saenphimmachak, C., Hoffman, L.R., D'Argenio, D.A., et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103 : 8487 8492.
59. Starkey, M., Hickman, J.H., Ma, L., Zhang, N., De Long, S., Hinz, A., et al. (2009) Pseudomonas aeruginosa rugose small colony variants have adaptations likely to promote persistence in the cystic fibrosis lung. J Bacteriol 191 : 3492 3503.
60. Thormann, K.M., Duttler, S., Saville, R.M., Hyodo, M., Shukla, S., Hayakawa, Y. Spormann, A.M. (2006) Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188 : 2681 2691.
61. Tischler, A.D. Camilli, A. (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53 : 857 869.
62. Tuomanen, E., Towbin, H., Rosenfelder, G., Braun, D., Larson, G., Hansson, G.C. Hill, R. (1988) Receptor analogs and monoclonal antibodies that inhibit adherence of Bordetella pertussis to human ciliated respiratory epithelial cells. J Exp Med 168 : 267 277.
63. Ulett, G.C., Valle, J., Beloin, C., Sherlock, O., Ghigo, J.M. Schembri, M.A. (2007) Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 75 : 3233 3244.
64. Vasseur, P., Vallet-Gely, I., Soscia, C., Genin, S. Filloux, A. (2005) The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151 : 985 997.
65. Vogel, H.J. Bonner, D.M. (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218 : 97 106.
66. Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C. Mattick, J.S. (2002) Extracellular DNA required for bacterial biofilm formation. Science 295 : 1487.
67. Willems, R.J., Geuijen, C., van der Heide, H.G., Renauld, G., Bertin, P., van den Akker, W.M., et al. (1994) Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol Microbiol 11 : 337 347.
68. Wolfgang, M.C., Kulasekara, B.R., Liang, X., Boyd, D., Wu, K., Yang, Q., et al. (2003) Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100 : 8484 8489.
69. Wu, S., Skolnick, J. Zhang, Y. (2007) Ab initio modeling of small proteins by iterative TASSER simulations. BMC Biol 5 : 17.
70. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9 : 40.