Characterization of temporal protein production in Pseudomonas aeruginosa biofilms

Journal of Bacteriology

Volumn 187, Issue 23, 2005, Pages 8114-8126

  Southey Pillig, Christopher J ^a   Davies, David G ^a   Sauer, Karin ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYTOCHROME C OXIDASE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BIOFILM; CCOO GENE; CHEMOTAXIS; GENE EXPRESSION; GENE MUTATION; NONHUMAN; PA4101 GENE; PA4208 GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BACTERIAL PROTEINS; BIOFILMS; GENES, BACTERIAL; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 28044459818     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.23.8114-8126.2005     Document Type: Article

References (74)

1. Aendekerk, S., B. Ghysels, P. Cornelis, and C. Baysse. 2002. Characterization of a new efflux pump, MexGHI-OpmD, from Pseudomonas aeruginosa that confers resistance to vanadium. Microbiology 148:2371-2381.
2. Aendekerk, S., S. P. Diggle, Z. Song, N. Hoiby, P. Cornelis, P. Williams, and M. Camara. 2005. The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151:1113-1125.
3. Allison, D. G. 2003. The biofilm matrix. Biofouling 19:139-150.
4. Alm, R. A., and J. S. Mattick. 1997. Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa. Gene 192:89-98.
5. Applegate, D. H., and J. D. Bryers. 1991. Effects on carbon and oxygen limitations and calcium concentrations on biofilm removal processes. Biotechnol. Bioeng. 37:17-25.
6. Bagge, N., M. Schuster, M. Hentzer, O. Ciofu, M. Givskov, E. P. Greenberg, and N. Hoiby. 2004. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob. Agents Chemother. 48:1175-1187.
7. Blum, H., H. Beier, and H. J. Gross. 1987. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93-99.
8. Bollinger, N., D. J. Hassett, B. H. Iglewski, J. W. Costerton, and T. R. McDermott. 2001. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J. Bacteriol. 183:1990-1996.
9. Ciofu, O., V. Fussing, N. Bagge, C. Koch, and N. Hoiby. 2001. Characterization of paired mucoid/non-mucoid Pseudomonas aeruginosa isolates from Danish cystic fibrosis patients: antibiotic resistance, beta-lactamase activity and RiboPrinting. J. Antimicrob. Chemother. 48:391-396.
10. Cochran, W. L., S. J. Suh, G. A. McFeters, and P. S. Stewart. 2000. Role of RpoS and AlgT in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide and monochloramine. J. Appl. Microbiol. 88:546-553.
11. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:318-322.
12. Costerton, J. W., Z. Lewandowski, D. DeBeer, D. Caldwell, D. Korber, and G. James. 1994. Biofilms, the customized microniche. J. Bacteriol. 176:2137-2142.
13. Cunin, R., N. Glansdorff, A. Pierard, and V. Stalon. 1986. Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50:314-352.
14. Dagastino, L., A. E. Goodman, and K. C. Marshall. 1991. Physiological responses induced in bacteria adhering to surfaces. Biofouling 4:113-119.
15. Dalaquis, P. J., D. E. Caldwell, J. R. Lawrence, and A. R. WcCurdy. 1989. Detachment of Pseudomonas fluorescens from biofilms on glass surfaces in response to nutrient stress. Microb. Ecol. 18:199-210.
16. Davies, D. G., and G. G. Geesey. 1995. Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl. Environ. Microbiol. 61:860-867.
17. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
18. Davey, M. E., and G. A. O'Toole. 2000. Microbiol biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847-867.
19. Doggett, R. G. 1969. Incidence of mucoid Pseudomonas aeruginosa from clinical sources. Appl. Microbiol. 18:936-937.
20. Dong, Y., Y. Y. Chen, J. A. Snyder, and R. A. Burne. 2002. Isolation and molecular analysis of the gene cluster for the arginine deiminase system from Streptococcus gordonii DL1. Appl. Environ. Microbiol. 68:5549-5553.
21. Drenkard, E. 2003. Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect. 5:1213-1219.
22. Ehrlich, G. D., R. Veeh, X. Wang, J. W. Costerton, J. D. Hayes, F. Z. Hu, B. J. Daigle, M. D. Ehrlich, and J. C. Post. 2002. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287:1710-1715.
23. Geesey, G. G., W. T. Richardson, H. G. Yeomans, R. T. Irvin, and J. W. Costerton. 1977. Microscopic examination of natural sessile bacterial populations from an alpine stream. Can. J. Microbiol. 23:1733-1736.
24. 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.
25. 54) in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185:2227-2235.
26. Heydorn, A., B. K. Ersboll, M. Hentzer, M. R. Parsek, M. Givskov, and S. Molin. 2000. Experimental reproducibility in flow-chamber biofilms. Microbiology 146:2409-2415.
27. Ishimoto, K. S., and S. Lory. 1989. Formation of pilin in Pseudomonas aeruginosa requires the alternative sigma factor (RpoN) of RNA polymerase. Proc. Natl. Acad. Sci. USA 86:1954-1957.
28. Jacobs, M. A., A. Alwood, I. Thaipisuttikul, D. Spencer, E. Haugen, S. Ernst, O. Will, R. Kaul, C. Raymond, R. Levy, L. Chun-Rong, D. Guenthner, D. Bovee, M. V. Olson, and C. Manoil. 2003. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 100:14339-14344.
29. James, G. A., D. R. Korber, D. E. Caldwell, and J. W. Costerton. 1995. Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp. J. Bacteriol. 177:907-915.
30. Jyot, J., N. Dasgupta, and R. Ramphal. 2002. FleQ, the major flagellar gene regulator in Pseudomonas aeruginosa, binds to enhancer sites located either upstream or atypically downstream of the RpoN binding site. J. Bacteriol. 184:5251-5260.
31. Kerr, C. J., K. S. Osborn, A. H. Rickard, G. D. Robson, and P. S. Handley. 2003. Biofilms in water distribution systems, p. 757-776. In M. Duncan and N. J. Horan (ed.), Water and wastewater engineering. Academic Press, London, United Kingdom.
32. Khoury, A. E., K. Lam, B. Ellis, and J. W. Costerton 1992. Prevention and control of bacterial infections associated with medical devices. ASAIO J. 38:M174-M178.
33. Kjelleberg, S., and S. Molin. 2002. Is there a role for quorum sensing signals in bacterial biofilms? Curr. Opin. Microbiol. 5:254-258.
34. 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.
35. Klausen, M., A. Heydorn, P. Ragas, L. Lambertsen, A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48:1511-1524.
36. 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.
37. Lamont, R. J., and H. F. Jenkinson. 1998. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62:1244-1263.
38. Marquis, R. E., G. R. Bender, D. R. Murray, and A. Wong. 1987. Arginine deiminase system and bacterial adaptation to acid environments. Appl. Environ. Microbiol. 53:198-200.
39. Marshall, J. C. 1988. Adhesion and growth of bacteria at surfaces in oligotrophic habitats. Can. J. Microbiol. 34:503-506.
40. Oosthuizen, M. C., B. Steyn, J. Theron, P. Cosette, D. Lindsay, A. Von Holy, and V. S. Brozel. 2002. Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl. Environ. Microbiol. 68:2770-2780.
41. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
42. O'Toole, G. A., K. A. Gibbs, P. W. Hager, P. V. Phibbs, Jr., and R. Kolter. 2000. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 182:425-431.
43. Otto, K., J. Norbeck, T. Larsson, K. A. Karlsson, and M. Hermansson. 2001. Adhesion of type 1-fimbriated Escherichia coli to abiotic surfaces leads to altered composition of outer membrane proteins. J. Bacteriol. 183:2445-2453.
44. Parkhill, J., B. W. Wren, K. Mungall, J. M. Ketley, C. Churcher, D. Basham, T. Chillingworth, R. M. Davies, T. Feltwell, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Moule, M. J. Pallen, C. W. Penn, M. A. Quail, M. A. Rajandream, K. M. Rutherford, A. H. van Vliet, S. Whitehead, and B. G. Barrell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
45. Parkins, M. D., H. Ceri, and D. G. Storey. 2001. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 40:1215-1226.
46. Pearson, J. P., C. Van Delden, and B. H. Iglewski. 1999. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 181:1203-1210.
47. Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83:346-356.
48. Pitcher, R. S., and N. J. Watmough. 2004. The bacterial cytochrome cbb3 oxidases. Biochim. Biophys. Acta 1655:388-399.
49. Preisig, O., D. Anthamatten, and H. Hennecke. 1993. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. USA 90:3309-3313.
50. Prigent-Combaret, C., O. Vidal, C. Dorel, and P. Lejeune. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181:5993-6002.
51. Ruiz-Manzano, A., L. Yuste, and F. Rojo. 2005. Levels and activity of the Pseudomonas putida global regulatory protein Crc vary according to growth conditions. J. Bacteriol. 187:3678-3686.
52. Sauer, K., A. K. Camper, G. D. Ehrlich, J. W. Costerton, and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes as a biofilm. J. Bacteriol. 184:1140-1154.
53. Sauer, K., and A. K. Camper. 2001. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183:6579-6589.
54. 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.
55. Sawyer, L. K., and S. W. Hermanowicz. 1998. Detachment of biofilm bacteria due to variations in nutrient supply. Water Sci. Technol. 37:211-214.
56. Schembri, M. A., K. Kjaergaard, and P. Klemm. 2003. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48:253-627.
57. Schuster, M., C. P. Lostroch, T. Ogi, and E. P. Greenberg. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:2066-2079.
58. Singh, P. K., A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762-764.
59. Singh, P. K., M. R. Parsek, E. P. Greenberg, and M. J. Welsh. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417:552-555.
60. Stanley, N. R., R. A. Britton, A. D. Grossman, and R. A. Lazazzera. 2003. Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J. Bacteriol. 185:1951-1957.
61. Stoodley, P., K. Sauer, D. G. Davies, and J. W. Costerton. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56:187-209.
62. Thormann, K. M., R. M. Seville, S. Shukla, and A. M. Spormann. 2005. Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J. Bacteriol. 187:1014-1021.
63. Tolker-Nielsen, T., and S. Molin. 2000. Spatial organization of microbial biofilm communities. Microb. Ecol. 40:75-84.
64. Tolker-Nielsen, T., U. C. Brinch, P. C. Ragas, J. B. Andersen, C. S. Jacobsen, and S. Molin. 2000. Development and dynamics of Pseudomonas sp. biofilms. J. Bacteriol. 182:6482-6489.
65. Tomb, J. F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, J. C. Venter, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
66. Totten, P. A., J. C. Lara, and S. Lory. 1990. The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J. Bacteriol. 172:389-396.
67. Wagner, V. E., D. Bushnell, L. Passador, A. I. Brooks, and B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environments. J. Bacteriol. 185:2080-2095.
68. Waite, R. D., A. Papakonstantinopoulon, E. Litter, and M. A. Curtis. 2005. Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J. Bacteriol. 187:6571-6576.
69. Webb, J. S., M. Lau, and S. Kjelleberg. 2004. Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186:8066-8073.
70. Werner, E., F. Roe, A. Bugnicourt, M. J. Franklin, A. Heydorn, S. Molin, B. Pitts, and P. S. Stewart. 2004. Stratified growth in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 70:6188-6196.
71. Whitchurch, C. B., T. E. Erova, J. A. Emery, J. L. Sargent, J. M. Harris, A. B. Semmler, M. D. Young, J. S. Mattick, and D. J. Wozniak. 2002. Phosphorylation of the Pseudomonas aeruginosa response regulator AlgR is essential for type IV fimbria-mediated twitching motility. J. Bacteriol. 184:4544-4554.
72. Whiteley, M., M. G. Bangera, R. E. Bumgarner, M. R. Parsek, G. M. Teitzel, S. Lory, and E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860-864.
73. Wimpenny, J. W. T. 2000. An overview of biofilms as functional communities, p. 1-24. In D. G. Allison, P. Gilbert, H. M. Lappin-Scott, and M. Wilson (ed.), Community structure and co-operation in biofilms. Cambridge University Press, Cambridge, United Kingdom.
74. Yoon, S. S., R. F. Hennigan, G. M. Hilliard, U. A. Ochsner, K. Parvatiyar, M. C. Kamani, H. L. Allen, T. R. DeKievit, P. R. Gardner, U. Schwab, J. J. Rowe, B. H. Iglewski, T. R. McDermott, R. P. Mason, D. J. Wozniak, R. E. Hancock, M. R. Parsek, T. L. Noah, R. C. Boucher, and D. J. Hassett. 2002. Pseudomonas aeruginosa anaerobic respiration in biofilms. Relationships to cystic fibrosis pathogenesis. Dev. Cell 3:593-603.