Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing

Environmental Microbiology

Volumn 6, Issue 3, 2004, Pages 218-226

  Matz, Carsten ^a   Bergfeld, Tanja ^a,b   Rice, Scott A ^a   Kjelleberg, Staffan ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b FEDERAL INSTITUTE OF HYDROLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; BACTERIAL PROTEIN; DNA BINDING PROTEIN; GLUCURONIC ACID; HEXURONIC ACID; LASR PROTEIN, PSEUDOMONAS AERUGINOSA; RHLR PROTEIN, PSEUDOMONAS AERUGINOSA; TRANSACTIVATOR PROTEIN;

ADAPTATION; ANIMAL; ARTICLE; BIOFILM; BIOSYNTHESIS; CYTOLOGY; FIMBRIA; FLAGELLATE; FLAGELLUM; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA;

ADAPTATION, BIOLOGICAL; ALGINATES; ANIMALS; BACTERIAL PROTEINS; BIOFILMS; DNA-BINDING PROTEINS; FIMBRIAE, BACTERIAL; FLAGELLA; GLUCURONIC ACID; HEXURONIC ACIDS; KINETOPLASTIDA; MICROSCOPY, FLUORESCENCE; MUTATION; PSEUDOMONAS AERUGINOSA; TRANS-ACTIVATORS;

ANIMALIA; BACTERIA (MICROORGANISMS); MASTIGOPHORA (FLAGELLATES); PROTOZOA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; RHYNCHOMONAS NASUTA;

EID: 1342332585     PISSN: 14622912     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2004.00556.x     Document Type: Article

References (43)

1. Arndt, H., Schmidt-Denter, K., Auer, B., and Weitere, M. (2003) Protozoans and biofilms. In Fossil and Recent Biofilms. Krumbein, W.E., Paterson, D.M., and Zavarzin, G.A., (eds). Dordrecht: Kluwer Academic Publishers, in press.
2. Beatson, S.A., Whitchurch, C.B., Semmler, A.B., and Mattick, J.S. (2002) Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J Bacteriol 184: 3598-3604.
3. Bodey, G.P., Bolivar, R., Fainstein, V., and Jadeja, L. (1993) Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 5: 270-313.
4. Botzenhart, K., and Döring, G. (1993) Ecology and epidemiology of Pseudomonas aeruginosa. In Pseudomonas aeruginosa as an Opportunistic Pathogen. Campa, M., Bendinelli, M., and Friedman, H., (eds). New York: Plenum Press, pp. 1-18.
5. Boyd, A., and Chakrabarty, A.M. (1995) Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J Ind Microbiol 15: 162-168.
6. Cosson, P., Zulianello, L., Join-Lambert, O., Faurisson, F., Gebbie, L., Benghezal, M., et al. (2002) Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 184: 3027-3033.
7. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., and Lappin-Scott, H.M. (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
8. Davey, M.E., and O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64: 847-867.
9. Davies, D.G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W., and Greenberg, E.P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295-298.
10. De Kievit, T.R., Gillis, R., Marx, S., Brown, C., and Iglewski, B.H. (2001) Quorum-sensing genes In Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67: 1865-1873.
11. Fenchel, T. (1987) Ecology of Protozoa: The Biology of Free-Living Phagotrophic Protists. Madison, WI: Science Tech Publishers.
12. Franklin, M., and Ohman, D. (1993) Identification of algF in the alginate biosynthetic gene cluster of Pseudomonas aeruginosa which is required for alginate acetylation. J Bacteriol 175: 5057-5065.
13. Gambello, M.J., and Iglewski, B.H. (1991) Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 173: 3000-3009.
14. Hahn, M.W., and Höfle, M.G. (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35: 113-121.
15. Hendrickson, E.L., Plotnikova, J., Mahajan-Miklos, S., Rahme, L.G., and Ausubel, F.M. (2001) Differential roles of the Pseudomonas aeruginosa PA14 rpoN gene in pathogenicity in plants, nematodes, insects, and mice. J Bacteriol 183: 7126-7134.
16. Hentzer, M., Teitzel, G.M., Balzer, G.J., Heydorn, A., Molin, S., Givskov, M., and Parsek, M.R. (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183: 5395-5401.
17. Heurlier, K., Dénervaud, V., Pessi, G., Reimmann, C., and Haas, D. (2003) Negative control of quorum sensing by RpoN (σ54) in Pseudomonas aeruginosa PAO1. J Bacteriol 185: 2227-2235.
18. Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersboll, B.K., and Molin, S. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407.
19. Heydorn, A., Ersboll, B., Kato, J., Hentzer, M., Parsek, M.R., Tolker-Nielsen, T., et al. (2002) Statistical analysis of Pseudomonas aeruginosa biofilm development: Impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Appl Environ Microbiol 68: 2008-2017.
20. Høiby, N., Johansen, H.K., Moser, C., Song, Z.J., Ciofu, O., and Kharazmi, A. (2001) Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 3: 23-35.
21. Jackson, S.M., and Jones, E.B.G. (1991) Interactions within biofilms: the disruption of biofilm structure by protozoa. Kieler Meeresforsch 8: 264-268.
22. Jürgens, K., and Matz, C. (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81: 413-434.
23. Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jorgensen, A., Molin, S., and Tolker-Nielsen, T. (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48: 1511-1524.
24. Krieg, D.P., Helmke, R.J., German, V.F., and Mangos, J.A. (1988) Resistance of mucoid Pseudomonas aeruginosa to nonopsonic phagocytosis by alveolar macrophages in vitro. Infect Immun 56: 3173-3179.
25. Lawrence, J.R., and Snyder, R.A. (1998) Feeding behaviour and grazing impacts of a Euplotes sp. on attached bacteria. Can J Microbiol 44: 623-629.
26. Mathee, K., Ciofu, O., Sternberg, C., Lindum, P.W., Campbell, J.I.A., Jensen, P., et al. (1999) Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145: 1349-1357.
27. Matz, C., and Jürgens, K. (2001) Effects of hydrophobic and electrostatic cell surface properties of bacteria on feeding rates of heterotrophic nanoflagellates. Appl Environ Microbiol 67: 814-820.
28. Matz, C., and Jürgens, K. (2003) Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb Ecol 45: 384-398.
29. Matz, C., Boenigk, J., Arndt, H., and Jürgens, K. (2002a) Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat Microb Ecol 27: 137-148.
30. Matz, C., Deines, P., and Jürgens, K. (2002b) Phenotypic variation in Pseudomonas sp CM10 determines microcolony formation and survival under protozoan grazing. FEMS Microbiol Ecol 39: 57-65.
31. O'Toole, G.A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
32. Patterson, D.J., and Lee, W.Y. (2000) Geographic distribution and diversity of free-living heterotrophic flagellates. In The Flagellates - Unity, Diversity and Evolution. Leadbeater, B.S.C. and Green, J.C., (eds). London: Taylor & Francis, pp. 269-287.
33. Pedersen, K. (1982) Factors regulating microbial biofilm development in a system with slowly flowing seawater. Appl Environ Microbiol 44: 1196-1204.
34. Pesci, E.C., and Iglewski, B.H. (1999) Quorum sensing in Pseudomonas aeruginosa. In Cell-Cell Signalling in Bacteria. Dunny, G.M., and Winans, S.C., (eds). Washington: D.C. American Society for Microbiology Press, pp. 147-155.
35. Pukatzki, S., Kessin, R.H., and Mekalanos, J.J. (2002) The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Nat Acad Sci USA 99: 3159-3164.
36. Ravn, L., Christensen, A.B., Molin, S., Givskov, M., and Gram, L. (2001) Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Meth 44: 239-251.
37. Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W., and Davies, D.G. (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184: 1140-1154.
38. Singh, P.K., Schaefer, A.L., Parsek, M.R., Moninger, T.O., Welsh, M.J., and Greenberg, E.P. (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762-764.
39. Spiers, A.J., Buckling, A., and Rainey, P.B. (2000) The causes of Pseudomonas diversity. Microbiology 146: 2345-2350.
40. Studholme, D.J., and Buck, M. (2000) The biology of enhancer-dependent transcriptional regulation in bacteria: insights from genome sequences. FEMS Microbiol Lett 186: 1-9.
41. Thompson, L.S., Webb, J.S., Rice, S.A., and Kjelleberg, S. (2003) The alternative sigma factor RpoN regulates the quorum sensing gene rhll in Pseudomonas aeruginosa. FEMS Microbiol Lett 220: 187-195.
42. Vaatanen, P. (1976) Microbiological studies on coastal waters of the Northern Baltic sea, I. Distribution and abundance of bacteria and yeasts in the Tvarminne area. Walter Andre Nottback Found Sci Rep 1: 1-58.
43. Webb, J.S., Thompson, L.S., James, S., Charlton, T., Tolker-Nielsen, T., Koch, B., et al. (2003) Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185: 4585-4592.