Identification of proteins associated with the pseudomonas aeruginosa biofilm extracellular matrix

Journal of Proteome Research

Volumn 11, Issue 10, 2012, Pages 4906-4915

  Toyofuku, Masanori ^a,d   Roschitzki, Bernd ^b   Riedel, Katharina ^c   Eberl, Leo ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Biofilm; Extracellular matrix; Membrane vesicle; P. aeruginosa

Indexed keywords

LIPID; MATRIX PROTEIN; NUCLEIC ACID; OUTER MEMBRANE PROTEIN; POLYSACCHARIDE;

ARTICLE; BIOFILM; ELECTRON MICROSCOPY; EXTRACELLULAR MATRIX; NONHUMAN; OUTER MEMBRANE; PLANKTON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PSEUDOMONAS AERUGINOSA; SESSILE SPECIES;

BACTERIAL OUTER MEMBRANE PROTEINS; BIOFILMS; CELL MEMBRANE; EXTRACELLULAR MATRIX; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PROTEOME; PSEUDOMONAS AERUGINOSA; SECRETORY VESICLES;

EID: 84867467871     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300395j     Document Type: Article

References (71)

1. Costerton, J. W.; Lewandowski, Z.; Caldwell, D. E.; Korber, D. R.; Lappin-Scott, H. M. Microbial biofilms Annu. Rev. Microbiol. 1995, 49, 711-745
2. Flemming, H. C.; Wingender, J. The biofilm matrix Nat. Rev. Microbiol. 2010, 8 (9) 623-633
3. Flemming, H. C.; Neu, T. R.; Wozniak, D. J. The EPS matrix: the "house of biofilm cells" J. Bacteriol. 2007, 189 (22) 7945-7947
4. Chapman, M. R.; Robinson, L. S.; Pinkner, J. S.; Roth, R.; Heuser, J.; Hammar, M.; Normark, S.; Hultgren, S. J. Role of Escherichia coli curli operons in directing amyloid fiber formation Science 2002, 295 (5556) 851-855
5. Romero, D.; Aguilar, C.; Losick, R.; Kolter, R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (5) 2230-2234
6. McSwain, B. S.; Irvine, R. L.; Hausner, M.; Wilderer, P. A. Composition and distribution of extracellular polymeric substances in aerobic flocs and granular sludge Appl. Environ. Microbiol. 2005, 71 (2) 1051-1057
7. Frlund, B.; Palmgren, R.; Keiding, K.; Nielsen, P. H. Extraction of extracellular polymers from activated sludge using a cation exchange resin Water Res. 1996, 30 (8) 1749-1758
8. Urbain, V.; Block, J. C.; Manem, J. Bioflocculation in Activated-Sludge: an Analytic Approach Water Res. 1993, 27 (5) 829-838
9. Govan, J. R.; Deretic, V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia Microbiol. Rev. 1996, 60 (3) 539-574
10. Friedman, L.; Kolter, R. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms Mol. Microbiol. 2004, 51 (3) 675-690
11. Jackson, K. D.; Starkey, M.; Kremer, S.; Parsek, M. R.; Wozniak, D. J. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation J. Bacteriol. 2004, 186 (14) 4466-4475
12. Matsukawa, M.; Greenberg, E. P. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development J. Bacteriol. 2004, 186 (14) 4449-4456
13. Friedman, L.; Kolter, R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix J. Bacteriol. 2004, 186 (14) 4457-4465
14. Ma, L.; Conover, M.; Lu, H.; Parsek, M. R.; Bayles, K.; Wozniak, D. J. Assembly and development of the Pseudomonas aeruginosa biofilm matrix PLoS Pathog. 2009, 5 (3) e1000354
15. Whitchurch, C. B.; Tolker-Nielsen, T.; Ragas, P. C.; Mattick, J. S. Extracellular DNA required for bacterial biofilm formation Science 2002, 295 (5559) 1487
16. Allesen-Holm, M.; Barken, K. B.; Yang, L.; Klausen, M.; Webb, J. S.; Kjelleberg, S.; Molin, S.; Givskov, M.; Tolker-Nielsen, T. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms Mol. Microbiol. 2006, 59 (4) 1114-1128
17. Borlee, B. R.; Goldman, A. D.; Murakami, K.; Samudrala, R.; Wozniak, D. J.; Parsek, M. R. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix Mol. Microbiol. 2010, 75 (4) 827-842
18. Tashiro, Y.; Uchiyama, H.; Nomura, N. Multifunctional membrane vesicles in Pseudomonas aeruginosa Environ. Microbiol. 2012, 14 (6) 1349-1362
19. Kulp, A.; Kuehn, M. J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles Annu. Rev. Microbiol. 2010, 64, 163-184
20. Mashburn-Warren, L. M.; Whiteley, M. Special delivery: vesicle trafficking in prokaryotes Mol. Microbiol. 2006, 61 (4) 839-846
21. Schooling, S. R.; Beveridge, T. J. Membrane vesicles: an overlooked component of the matrices of biofilms J. Bacteriol. 2006, 188 (16) 5945-5957
22. Rani, S. A.; Pitts, B.; Beyenal, H.; Veluchamy, R. A.; Lewandowski, Z.; Davison, W. M.; Buckingham-Meyer, K.; Stewart, P. S. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states J. Bacteriol. 2007, 189 (11) 4223-4233
23. Wingender, J.; Strathmann, M.; Rode, A.; Leis, A.; Flemming, H. C. Isolation and biochemical characterization of extracellular polymeric substances from Pseudomonas aeruginosa Methods Enzymol. 2001, 336, 302-314
24. Hurkman, W. J.; Tanaka, C. K. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis Plant Physiol. 1986, 81 (3) 802-806
25. Tashiro, Y.; Sakai, R.; Toyofuku, M.; Sawada, I.; Nakajima-Kambe, T.; Uchiyama, H.; Nomura, N. Outer membrane machinery and alginate synthesis regulators control membrane vesicle production in Pseudomonas aeruginosa J. Bacteriol. 2009, 191 (24) 7509-7519
26. Tashiro, Y.; Ichikawa, S.; Shimizu, M.; Toyofuku, M.; Takaya, N.; Nakajima-Kambe, T.; Uchiyama, H.; Nomura, N. Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa Appl. Environ. Microbiol. 2010, 76 (11) 3732-3739
27. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
28. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970, 227 (5259) 680-685
29. Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250 Electrophoresis 1988, 9 (6) 255-262
30. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 1996, 68 (5) 850-858
31. Vizcaíno, J. A.; Côté, R.; Reisinger, F.; Barsnes, H.; Foster, J. M.; Rameseder, J.; Hermjakob, H.; Martens, L. The Proteomics Identifications database: 2010 update Nucleic Acids Res. 2010, 38 (Database issue) D736-42
32. Barsnes, H.; Vizcaíno, J. A.; Eidhammer, I.; Martens, L. PRIDE Converter: making proteomics data-sharing easy Nat. Biotechnol. 2009, 27 (7) 598-599
33. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4 (3) 207-214
34. Yu, N. Y.; Wagner, J. R.; Laird, M. R.; Melli, G.; Rey, S.; Lo, R.; Dao, P.; Sahinalp, S. C.; Ester, M.; Foster, L. J.; Brinkman, F. S. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes Bioinformatics 2010, 26 (13) 1608-1615
35. Lee, E. Y.; Bang, J. Y.; Park, G. W.; Choi, D. S.; Kang, J. S.; Kim, H. J.; Park, K. S.; Lee, J. O.; Kim, Y. K.; Kwon, K. H.; Kim, K. P.; Gho, Y. S. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli Proteomics 2007, 7 (17) 3143-3153
36. Schooling, S. R.; Hubley, A.; Beveridge, T. J. Interactions of DNA with biofilm-derived membrane vesicles J. Bacteriol. 2009, 191 (13) 4097-4102
37. Srinivas, N.; Jetter, P.; Ueberbacher, B. J.; Werneburg, M.; Zerbe, K.; Steinmann, J.; Van der Meijden, B.; Bernardini, F.; Lederer, A.; Dias, R. L.; Misson, P. E.; Henze, H.; Zumbrunn, J.; Gombert, F. O.; Obrecht, D.; Hunziker, P.; Schauer, S.; Ziegler, U.; Käch, A.; Eberl, L.; Riedel, K.; DeMarco, S. J.; Robinson, J. A. Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa Science 2010, 327 (5968) 1010-1013
38. Choi, D. S.; Kim, D. K.; Choi, S. J.; Lee, J.; Choi, J. P.; Rho, S.; Park, S. H.; Kim, Y. K.; Hwang, D.; Gho, Y. S. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa Proteomics 2011, 11 (16) 3424-3429
39. Bauman, S. J.; Kuehn, M. J. Pseudomonas aeruginosa vesicles associate with and are internalized by human lung epithelial cells BMC Microbiol. 2009, 9, 26
40. Bomberger, J. M.; Maceachran, D. P.; Coutermarsh, B. A.; Ye, S.; OToole, G. A.; Stanton, B. A. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles PLoS Pathog. 2009, 5 (4) e1000382
41. Ellis, T. N.; Leiman, S. A.; Kuehn, M. J. Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components Infect. Immunol. 2010, 78 (9) 3822-3831
42. Kadurugamuwa, J. L.; Beveridge, T. J. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion J. Bacteriol. 1995, 177 (14) 3998-4008
43. Jiao, Y.; DHaeseleer, P.; Dill, B. D.; Shah, M.; Verberkmoes, N. C.; Hettich, R. L.; Banfield, J. F.; Thelen, M. P. Identification of biofilm matrix-associated proteins from an acid mine drainage microbial community Appl. Environ. Microbiol. 2011, 77 (15) 5230-5237
44. Gallaher, T. K.; Wu, S.; Webster, P.; Aguilera, R. Identification of biofilm proteins in non-typeable Haemophilus Influenzae BMC Microbiol. 2006, 6, 65
45. Curtis, P. D.; Atwood, J., 3rd; Orlando, R.; Shimkets, L. J. Proteins associated with the Myxococcus xanthus extracellular matrix J. Bacteriol. 2007, 189 (21) 7634-7642
46. Eboigbodin, K. E.; Biggs, C. A. Characterization of the extracellular polymeric substances produced by Escherichia coli using infrared spectroscopic, proteomic, and aggregation studies Biomacromolecules 2008, 9 (2) 686-695
47. Park, C.; Novak, J. T.; Helm, R. F.; Ahn, Y. O.; Esen, A. Evaluation of the extracellular proteins in full-scale activated sludges Water Res. 2008, 42 (14) 3879-3889
48. Webb, J. S.; Thompson, L. S.; James, S.; Charlton, T.; Tolker-Nielsen, T.; Koch, B.; Givskov, M.; Kjelleberg, S. Cell death in Pseudomonas aeruginosa biofilm development J. Bacteriol. 2003, 185 (15) 4585-4592
49. Hentzer, M.; Wu, H.; Andersen, J. B.; Riedel, K.; Rasmussen, T. B.; Bagge, N.; Kumar, N.; Schembri, M. A.; Song, Z.; Kristoffersen, P.; Manefield, M.; Costerton, J. W.; Molin, S.; Eberl, L.; Steinberg, P.; Kjelleberg, S.; Hiby, N.; Givskov, M. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors EMBO J. 2003, 22 (15) 3803-3815
50. Rao, J.; DiGiandomenico, A.; Artamonov, M.; Leitinger, N.; Amin, A. R.; Goldberg, J. B. Host derived inflammatory phospholipids regulate rahU (PA0122) gene, protein, and biofilm formation in Pseudomonas aeruginosa Cell Immunol. 2011, 270 (2) 95-102
51. Relman, D. A.; Domenighini, M.; Tuomanen, E.; Rappuoli, R.; Falkow, S. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence Proc. Natl. Acad. Sci. U.S.A. 1989, 86 (8) 2637-2641
52. Lasa, I.; Penadés, J. R. Bap: a family of surface proteins involved in biofilm formation Res. Microbiol. 2006, 157 (2) 99-107
53. Hassett, D. J.; Alsabbagh, E.; Parvatiyar, K.; Howell, M. L.; Wilmott, R. W.; Ochsner, U. A. A protease-resistant catalase, KatA, released upon cell lysis during stationary phase is essential for aerobic survival of a Pseudomonas aeruginosa oxyR mutant at low cell densities J. Bacteriol. 2000, 182 (16) 4557-4563
54. Hassett, D. J.; Ma, J. F.; Elkins, J. G.; McDermott, T. R.; Ochsner, U. A.; West, S. E.; Huang, C. T.; Fredericks, J.; Burnett, S.; Stewart, P. S.; McFeters, G.; Passador, L.; Iglewski, B. H. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide Mol. Microbiol. 1999, 34 (5) 1082-1093
55. Stewart, P. S.; Roe, F.; Rayner, J.; Elkins, J. G.; Lewandowski, Z.; Ochsner, U. A.; Hassett, D. J. Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms Appl. Environ. Microbiol. 2000, 66 (2) 836-838
56. Hassett, D. J.; Cohen, M. S. Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells FASEB J. 1989, 3 (14) 2574-2582
57. Jeffery, C. J. Moonlighting proteins: old proteins learning new tricks Trends Genet. 2003, 19 (8) 415-417
58. Kunert, A.; Losse, J.; Gruszin, C.; Hühn, M.; Kaendler, K.; Mikkat, S.; Volke, D.; Hoffmann, R.; Jokiranta, T. S.; Seeberger, H.; Moellmann, U.; Hellwage, J.; Zipfel, P. F. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein J. Immunol. 2007, 179 (5) 2979-2988
59. Bergonzelli, G. E.; Granato, D.; Pridmore, R. D.; Marvin-Guy, L. F.; Donnicola, D.; Corthésy-Theulaz, I. E. GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori Infect. Immunol. 2006, 74 (1) 425-34
60. Granato, D.; Bergonzelli, G. E.; Pridmore, R. D.; Marvin, L.; Rouvet, M.; Corthésy-Theulaz, I. E. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins Infect. Immunol. 2004, 72 (4) 2160-2169
61. Dillon, S. C.; Dorman, C. J. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression Nat. Rev. Microbiol. 2010, 8 (3) 185-195
62. Mulcahy, H.; Charron-Mazenod, L.; Lewenza, S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms PLoS Pathog. 2008, 4 (11) e1000213
63. Sidhu, V. K.; Vorhölter, F. J.; Niehaus, K.; Watt, S. A. Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris BMC Microbiol. 2008, 8, 87
64. Bauman, S. J.; Kuehn, M. J. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response Microbes Infect. 2006, 8 (9-10) 2400-2408
65. OToole, G. A. Microbiology: Jekyll or hide? Nature 2004, 432 (7018) 680-681
66. Goodman, A. L.; Kulasekara, B.; Rietsch, A.; Boyd, D.; Smith, R. S.; Lory, S. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa Dev. Cell 2004, 7 (5) 745-754
67. Patriquin, G. M.; Banin, E.; Gilmour, C.; Tuchman, R.; Greenberg, E. P.; Poole, K. Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa J. Bacteriol. 2008, 190 (2) 662-671
68. Berlutti, F.; Morea, C.; Battistoni, A.; Sarli, S.; Cipriani, P.; Superti, F.; Ammendolia, M. G.; Valenti, P. Iron availability influences aggregation, biofilm, adhesion and invasion of Pseudomonas aeruginosa and Burkholderia cenocepacia Int. J. Immunopathol. Pharmacol. 2005, 18 (4) 661-870
69. Banin, E.; Vasil, M. L.; Greenberg, E. P. Iron and Pseudomonas aeruginosa biofilm formation Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (31) 11076-11081
70. Singh, P. K.; Parsek, M. R.; Greenberg, E. P.; Welsh, M. J. A component of innate immunity prevents bacterial biofilm development Nature 2002, 417 (6888) 552-555
71. Hentzer, M.; Eberl, L.; Givskov, M. Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation Biofilms 2005, 2, 37-61