Previous Article | Next Article 
Applied and Environmental Microbiology, August 2006, p. 5414-5420, Vol. 72, No. 8
0099-2240/06/$08.00+0 doi:10.1128/AEM.00546-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
Ecological Advantages of Autolysis during the Development and Dispersal of Pseudoalteromonas tunicata Biofilms
Anne Mai-Prochnow,1
Jeremy S. Webb,1,
Belinda C. Ferrari,2 and
Staffan Kjelleberg1*
School of Biotechnology and Biomolecular Sciences and Centre for Marine Biofouling and Bio-innovation, University of New South Wales, Sydney, NSW 2052, Australia,1
Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, NSW 2109, Australia2
Received 7 March 2006/
Accepted 24 May 2006
In the ubiquitous marine bacterium Pseudoalteromonas tunicata, subpopulations of cells are killed by the production of an autocidal protein, AlpP, during biofilm development. Our data demonstrate an involvement of this process in two parameters, dispersal and phenotypic diversification, which are of importance for the ecology of this organism and for its survival within the environment. Cell death in P. tunicata wild-type biofilms led to a major reproducible dispersal event after 192 h of biofilm development. The dispersal was not observed with a
AlpP mutant strain. Using flow cytometry and the fluorescent dye DiBAC4(3), we also show that P. tunicata wild-type cells that disperse from biofilms have enhanced metabolic activity compared to those cells that disperse from
AlpP mutant biofilms, possibly due to nutrients released from dead cells. Furthermore, we report that there was considerable phenotypic variation among cells dispersing from wild-type biofilms but not from the
AlpP mutant. Wild-type cells that dispersed from biofilms showed significantly increased variations in growth, motility, and biofilm formation, which may be important for successful colonization of new surfaces. These findings suggest for the first time that the autocidal events mediated by an antibacterial protein can confer ecological advantages to the species by generating a metabolically active and phenotypically diverse subpopulation of dispersal cells.
* Corresponding author. Mailing address: School of Biotechnology and Biomolecular Sciences and Centre for Marine Biofouling and Bio-innovation, Biological Sciences Building, University of New South Wales, Kensington, Sydney, NSW 2052, Australia. Phone: 61 (2) 9385 2102/2276. Fax: 61 (2) 9385 1779. E-mail:
s.kjelleberg{at}unsw.edu.au.
Present address: School of Biological Sciences, University of South Hampton, South Hampton S016 7PS, United Kingdom.
Applied and Environmental Microbiology, August 2006, p. 5414-5420, Vol. 72, No. 8
0099-2240/06/$08.00+0 doi:10.1128/AEM.00546-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Kreth, J., Vu, H., Zhang, Y., Herzberg, M. C.
(2009). Characterization of Hydrogen Peroxide-Induced DNA Release by Streptococcus sanguinis and Streptococcus gordonii. J. Bacteriol.
191: 6281-6291
[Abstract]
[Full Text]
-
Karatan, E., Watnick, P.
(2009). Signals, Regulatory Networks, and Materials That Build and Break Bacterial Biofilms. Microbiol. Mol. Biol. Rev.
73: 310-347
[Abstract]
[Full Text]
-
Kim, Y., Wang, X., Ma, Q., Zhang, X.-S., Wood, T. K.
(2009). Toxin-Antitoxin Systems in Escherichia coli Influence Biofilm Formation through YjgK (TabA) and Fimbriae. J. Bacteriol.
191: 1258-1267
[Abstract]
[Full Text]
-
Chia, N., Woese, C. R., Goldenfeld, N.
(2008). A collective mechanism for phase variation in biofilms. Proc. Natl. Acad. Sci. USA
105: 14597-14602
[Abstract]
[Full Text]
-
Mai-Prochnow, A., Lucas-Elio, P., Egan, S., Thomas, T., Webb, J. S., Sanchez-Amat, A., Kjelleberg, S.
(2008). Hydrogen Peroxide Linked to Lysine Oxidase Activity Facilitates Biofilm Differentiation and Dispersal in Several Gram-Negative Bacteria. J. Bacteriol.
190: 5493-5501
[Abstract]
[Full Text]
-
Krupovic, M., Daugelavicius, R., Bamford, D. H.
(2007). Polymyxin B Induces Lysis of Marine Pseudoalteromonads. Antimicrob. Agents Chemother.
51: 3908-3914
[Abstract]
[Full Text]
-
Kirov, S. M., Webb, J. S., O'May, C. Y., Reid, D. W., Woo, J. K. K., Rice, S. A., Kjelleberg, S.
(2007). Biofilm differentiation and dispersal in mucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology
153: 3264-3274
[Abstract]
[Full Text]
-
Merod, R. T., Warren, J. E., McCaslin, H., Wuertz, S.
(2007). Toward Automated Analysis of Biofilm Architecture: Bias Caused by Extraneous Confocal Laser Scanning Microscopy Images. Appl. Environ. Microbiol.
73: 4922-4930
[Abstract]
[Full Text]
-
Rice, K. C., Mann, E. E., Endres, J. L., Weiss, E. C., Cassat, J. E., Smeltzer, M. S., Bayles, K. W.
(2007). The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA
104: 8113-8118
[Abstract]
[Full Text]
-
Koh, K. S., Lam, K. W., Alhede, M., Queck, S. Y., Labbate, M., Kjelleberg, S., Rice, S. A.
(2007). Phenotypic Diversification and Adaptation of Serratia marcescens MG1 Biofilm-Derived Morphotypes. J. Bacteriol.
189: 119-130
[Abstract]
[Full Text]
-
Barraud, N., Hassett, D. J., Hwang, S.-H., Rice, S. A., Kjelleberg, S., Webb, J. S.
(2006). Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa.. J. Bacteriol.
188: 7344-7353
[Abstract]
[Full Text]