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Journal of Bacteriology, December 2004, p. 8066-8073, Vol. 186, No. 23
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.23.8066-8073.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Bacteriophage and Phenotypic Variation in Pseudomonas aeruginosa Biofilm Development

Jeremy S. Webb,1,{dagger} Mathew Lau,1,2,{dagger}* and Staffan Kjelleberg1

School of Biotechnology and Biomolecular Sciences and Centre for Marine Biofouling and Bio-innovation, University of New South Wales, Sydney, Australia,1 School of Chemical and Life Sciences, Nanyang Polytechnic, Singapore, Singapore2

Received 19 August 2004/ Accepted 24 August 2004

A current question in biofilm research is whether biofilm-specific genetic processes can lead to differentiation in physiology and function among biofilm cells. In Pseudomonas aeruginosa, phenotypic variants which exhibit a small-colony phenotype on agar media and a markedly accelerated pattern of biofilm development compared to that of the parental strain are often isolated from biofilms. We grew P. aeruginosa biofilms in glass flow cell reactors and observed that the emergence of small-colony variants (SCVs) in the effluent runoff from the biofilms correlated with the emergence of plaque-forming Pf1-like filamentous phage (designated Pf4) from the biofilm. Because several recent studies have shown that bacteriophage genes are among the most highly upregulated groups of genes during biofilm development, we investigated whether Pf4 plays a role in SCV formation during P. aeruginosa biofilm development. We carried out immunoelectron microscopy using anti-Pf4 antibodies and observed that SCV cells, but not parental-type cells, exhibited high densities of Pf4 filaments on the cell surface and that these filaments were often tightly interwoven into complex latticeworks surrounding the cells. Moreover, infection of P. aeruginosa planktonic cultures with Pf4 caused the emergence of SCVs within the culture. These SCVs exhibited enhanced attachment, accelerated biofilm development, and large regions of dead and lysed cells inside microcolonies in a manner identical to that of SCVs obtained from biofilms. We concluded that Pf4 can mediate phenotypic variation in P. aeruginosa biofilms. We also performed partial sequencing and analysis of the Pf4 replicative form and identified a number of open reading frames not previously recognized in the genome of P. aeruginosa, including a putative postsegregational killing operon.

* Corresponding author. Mailing address: School of Chemical and Life Sciences, Nanyang Polytechnic, 180 Ang Mo Kio Ave. 8, Singapore 569830. Phone: 65 6550 1536. Fax: 65 6552 0844. E-mail: Mathew_LAU{at}nyp.gov.sg.

{dagger} J.S.W. and M.L. contributed equally to this work

Journal of Bacteriology, December 2004, p. 8066-8073, Vol. 186, No. 23
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.23.8066-8073.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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