Cell Death in Pseudomonas aeruginosa Biofilm Development

Journal of Bacteriology - Tập 185 Số 15 - Trang 4585-4592 - 2003
Jeremy S. Webb1, Lyndal S. Thompson1, S. R. James1, Tim Charlton1, Tim Tolker‐Nielsen2, Birgit Koch2, Michael Givskov2, Staffan Kjelleberg1
1School of Biotechnology and Biomolecular Sciences, and Centre for Marine Biofouling and Bio-innovation, University of New South Wales, Sydney, NSW 2052, Australia
2BioCentrum, Technical University of Denmark, DK-2800 Lyngby, Denmark

Tóm tắt

ABSTRACT Bacteria growing in biofilms often develop multicellular, three-dimensional structures known as microcolonies. Complex differentiation within biofilms of Pseudomonas aeruginosa occurs, leading to the creation of voids inside microcolonies and to the dispersal of cells from within these voids. However, key developmental processes regulating these events are poorly understood. A normal component of multicellular development is cell death. Here we report that a repeatable pattern of cell death and lysis occurs in biofilms of P. aeruginosa during the normal course of development. Cell death occurred with temporal and spatial organization within biofilms, inside microcolonies, when the biofilms were allowed to develop in continuous-culture flow cells. A subpopulation of viable cells was always observed in these regions. During the onset of biofilm killing and during biofilm development thereafter, a bacteriophage capable of superinfecting and lysing the P. aeruginosa parent strain was detected in the fluid effluent from the biofilm. The bacteriophage implicated in biofilm killing was closely related to the filamentous phage Pf1 and existed as a prophage within the genome of P. aeruginosa . We propose that prophage-mediated cell death is an important mechanism of differentiation inside microcolonies that facilitates dispersal of a subpopulation of surviving cells.

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Tài liệu tham khảo

10.1128/AEM.64.6.2240-2246.1998

Auschill, T. M., N. B. Arweiler, L. Netuschil, M. Brecx, E. Reich, A. Sculean, and N. B. Artweiler. 2001. Spatial distribution of vital and dead microorganisms in dental biofilms. Arch. Oral Biol.46:471-476.

Ausubel F. M. R. Brent R. E. Kingston D. D. Moore J. G. Seidman J. A. Smith and K. Struhl. 1992. Short protocols in molecular biology. Greene Publishing and John Wiley & Sons New York N.Y.

10.1128/JB.184.13.3598-3604.2002

Berk, R. S. 1965. Effect of antibacterial agents on the autoplaque phenomenon of Pseudomonas aeruginosa. Can. J. Microbiol.11:213-219.

10.1128/jb.86.4.728-734.1963

10.1128/jb.177.24.7155-7163.1995

Cheng, C. M., H. J. Wang, H. J. Bau, and T. T. Kuo. 1999. The primary immunity determinant in modulating the lysogenic immunity of the filamentous bacteriophage cf. J. Mol. Biol.287:867-876.

10.1126/science.284.5418.1318

10.1128/JB.182.12.3593-3596.2000

10.1128/JB.184.23.6481-6489.2002

10.1128/JB.185.3.1027-1036.2003

10.1126/science.280.5361.295

Debeer, D., P. Stoodley, F. Roe, and Z. Lewandowski. 1994. Effects of biofilm structures on oxygen distribution and mass-transport. Biotechnol. Bioeng.43:1131-1138.

Demple, B., and L. Harrison. 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem.63:915-948.

Doi R. H. 1989. Sporulation and germination p. 167-215. In C. R. Harwood (ed.) Bacillus . Plenum Press London United Kingdom.

Eisenstark A. 1967. Bacteriophage techniques p. 449-524. In K. Maramorosch and H. Koprowski (ed.) Methods in virology vol. 1. Academic Press New York N.Y.

Ellis, R. E., J. Y. Yuan, and H. R. Horvitz. 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol.7:663-698.

Engelberg-Kulka, H., and G. Glaser. 1999. Addiction modules and programmed cell death and antideath in bacterial cultures. Annu. Rev. Microbiol.53:43-70.

10.1128/mr.55.4.561-585.1991

10.1128/JB.182.9.2438-2444.2000

10.1128/JB.180.22.5896-5905.1998

Herrero, M., V. de Lorenzo, and K. N. Timmis. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol.172:6557-6567.

Hill, D. F., N. J. Short, R. N. Perham, and G. B. Petersen. 1991. DNA sequence of the filamentous bacteriophage Pf1. J. Mol. Biol.218:349-364.

Hoiby, N., H. Krogh Johansen, C. Moser, Z. Song, O. Ciofu, and A. Kharazmi. 2001. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect.3:23-35.

10.1128/br.33.3.419-443.1969

Hope, C. K., D. Clements, and M. Wilson. 2002. Determining the spatial distribution of viable and nonviable bacteria in hydrated microcosm dental plaques by viability profiling. J. Appl. Microbiol.93:448-455.

Huber, B., K. Riedel, M. Hentzer, A. Heydorn, A. Gotschlich, M. Givskov, S. Molin, and L. Eberl. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology147:2517-2528.

10.1128/JB.185.8.2628-2634.2003

Klausen M. A. Heydorn P. Ragas L. Lambertsen A. Aaes-Jorgensen S. Molin and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wildtype flagella and type IV pili mutants. Mol. Microbiol. 48: 1511-1524.

Konola, J. T., K. E. Sargent, and J. B. Gow. 2000. Efficient repair of hydrogen peroxide-induced DNA damage by Escherichia coli requires SOS induction of RecA and RuvA proteins. Mutat. Res.459:187-194.

Kuo, M. Y., M. K. Yang, W. P. Chen, and T. T. Kuo. 2000. High-frequency interconversion of turbid and clear plaque strains of bacteriophage f1 and associated host cell death. Can. J. Microbiol.46:841-847.

Kuo, T. T., C. C. Chiang, S. Y. Chen, J. H. Lin, and J. L. Kuo. 1994. A long lytic cycle in filamentous phage Cf1tv infecting Xanthomonas campestris pv. citri. Arch. Virol.135:253-264.

10.1128/jb.173.20.6558-6567.1991

10.1128/MMBR.64.3.503-514.2000

10.1006/jmbi.1998.2163

10.1128/jb.179.9.2845-2851.1997

Lynch, M. J., S. Swift, D. F. Kirke, C. W. Keevil, C. E. Dodd, and P. Williams. 2002. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol.4:18-28.

Maniatis T. E. F. Fritsch and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.

Marvin, D. A. 1998. Filamentous phage structure, infection and assembly. Curr. Opin. Struct. Biol.8:150-158.

10.1128/br.33.2.172-209.1969

McKenzie, G. J., R. S. Harris, P. L. Lee, and S. M. Rosenberg. 2000. The SOS response regulates adaptive mutation. Proc. Natl. Acad. Sci. USA97:6646-6651.

Meier, P., A. Finch, and G. Evan. 2000. Apoptosis in development. Nature407:796-801.

Merino, S., S. Camprubi, and J. M. Tomas. 1990. Isolation and characterization of bacteriophage PM3 from Aeromonas hydrophila, the bacterial receptor for which is the monopolar flagellum. FEMS Microbiol. Lett.57:277-282.

10.1128/AEM.64.2.721-732.1998

10.1128/jb.179.18.5756-5767.1997

Ptashne M. 1987. A genetic switch. Blackwell Scientific Cambridge United Kingdom.

Raff, M. C. 1992. Social controls on cell survival and cell death. Nature356:397-400.

Rashid, M. H., and A. Kornberg. 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA97:4885-4890.

10.1128/jb.172.8.4307-4314.1990

10.1128/jb.184.4.1140-1154.2002

Schweizer, H. P. 1992. Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol. Microbiol.6:1195-1204.

Shieh, G. J., Y. C. Charng, B. C. Yang, T. Jenn, H. J. Bau, and T. T. Kuo. 1991. Identification and nucleotide sequence analysis of an open reading frame involved in high-frequency conversion of turbid to clear plaque mutants of filamentous phage Cf1t. Virology185:316-322.

Shimkets, L. J. 1999. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol.53:525-549.

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. Nature407:762-764.

Steinmoen, H., E. Knutsen, and L. S. Havarstein. 2002. Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc. Natl. Acad. Sci. USA99:7681-7686.

Steller, H. 1995. Mechanisms and genes of cellular suicide. Science267:1445-1449.

10.1128/AEM.65.9.4108-4117.1999

Stoodley, P., K. Sauer, D. G. Davies, and J. W. Costerton. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol.56:187-209.

Taddei, F., I. Matic, and M. Radman. 1995. cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proc. Natl. Acad. Sci. USA92:11736-11740.

Thompson, L. S., J. S. Webb, S. A. Rice, and S. Kjelleberg. 2003. The alternative sigma factor RpoN regulates rhlI expression in Pseudomonas aeruginosa. FEMS Microbiol. Lett.220:187-195.

10.1128/jb.172.1.389-396.1990

Vaux, D. L., G. Haecker, and A. Strasser. 1994. An evolutionary perspective on apoptosis. Cell76:777-779.

10.1128/JB.185.7.2080-2095.2003

Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol.34:586-595.

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. Nature413:860-864.

10.1128/jb.129.2.798-802.1977

Wireman, J. W., and M. Dworkin. 1975. Morphogenesis and developmental interactions in myxobacteria. Science189:516-523.

10.1128/jb.179.24.7748-7758.1997

Yamamoto, K. R., B. M. Alberts, R. Benzinger, L. Lawhorne, and G. Treiber. 1970. Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology40:734-744.