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Journal of Bacteriology, November 2006, p. 7344-7353, Vol. 188, No. 21
0021-9193/06/$08.00+0     doi:10.1128/JB.00779-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa

Nicolas Barraud,1 Daniel J. Hassett,2 Sung-Hei Hwang,2 Scott A. Rice,1 Staffan Kjelleberg,1* and Jeremy S. Webb1,3

School of Biotechnology and Biomolecular Sciences, Centre for Marine Biofouling and Bio-innovation, and Environmental Biotechnology Cooperative Research Centre, University of New South Wales, Sydney, NSW 2052, Australia,1 Department of Molecular Genetics, Biochemistry and Microbiology, University of Cincinnati College of Medicine, Cincinnati, Ohio 45267,2 School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton SO16 7PX, United Kingdom3

Received 31 May 2006/ Accepted 27 July 2006

Bacterial biofilms at times undergo regulated and coordinated dispersal events where sessile biofilm cells convert to free-swimming, planktonic bacteria. In the opportunistic pathogen Pseudomonas aeruginosa, we previously observed that dispersal occurs concurrently with three interrelated processes within mature biofilms: (i) production of oxidative or nitrosative stress-inducing molecules inside biofilm structures, (ii) bacteriophage induction, and (iii) cell lysis. Here we examine whether specific reactive oxygen or nitrogen intermediates play a role in cell dispersal from P. aeruginosa biofilms. We demonstrate the involvement of anaerobic respiration processes in P. aeruginosa biofilm dispersal and show that nitric oxide (NO), used widely as a signaling molecule in biological systems, causes dispersal of P. aeruginosa biofilm bacteria. Dispersal was induced with low, sublethal concentrations (25 to 500 nM) of the NO donor sodium nitroprusside (SNP). Moreover, a P. aeruginosa mutant lacking the only enzyme capable of generating metabolic NO through anaerobic respiration (nitrite reductase, {Delta}nirS) did not disperse, whereas a NO reductase mutant ({Delta}norCB) exhibited greatly enhanced dispersal. Strategies to induce biofilm dispersal are of interest due to their potential to prevent biofilms and biofilm-related infections. We observed that exposure to SNP (500 nM) greatly enhanced the efficacy of antimicrobial compounds (tobramycin, hydrogen peroxide, and sodium dodecyl sulfate) in the removal of established P. aeruginosa biofilms from a glass surface. Combined exposure to both NO and antimicrobial agents may therefore offer a novel strategy to control preestablished, persistent P. aeruginosa biofilms and biofilm-related infections.

* 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. Fax: 61 (2) 9385 1779. E-mail: s.kjelleberg{at}unsw.edu.au.

Journal of Bacteriology, November 2006, p. 7344-7353, Vol. 188, No. 21
0021-9193/06/$08.00+0     doi:10.1128/JB.00779-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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