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Journal of Bacteriology, August 2008, p. 5493-5501, Vol. 190, No. 15
0021-9193/08/$08.00+0     doi:10.1128/JB.00549-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Hydrogen Peroxide Linked to Lysine Oxidase Activity Facilitates Biofilm Differentiation and Dispersal in Several Gram-Negative Bacteria{triangledown}

Anne Mai-Prochnow,1,{dagger} Patricia Lucas-Elio,2,{dagger} Suhelen Egan,1 Torsten Thomas,1 Jeremy S. Webb,1,3 Antonio Sanchez-Amat,2 and Staffan Kjelleberg1*

School of Biotechnology and Biomolecular Sciences and Centre for Marine Bio-Innovation, University of New South Wales, Sydney, NSW 2052, Australia,1 Department of Genetics and Microbiology, University of Murcia, 30100 Murcia, Spain,2 School of Biological Sciences, University of Southampton, Southampton SO16 7PX, United Kingdom3

Received 21 April 2008/ Accepted 16 May 2008

The marine bacterium Pseudoalteromonas tunicata produces an antibacterial and autolytic protein, AlpP, which causes death of a subpopulation of cells during biofilm formation and mediates differentiation, dispersal, and phenotypic variation among dispersal cells. The AlpP homologue (LodA) in the marine bacterium Marinomonas mediterranea was recently identified as a lysine oxidase which mediates cell death through the production of hydrogen peroxide. Here we show that AlpP in P. tunicata also acts as a lysine oxidase and that the hydrogen peroxide generated is responsible for cell death within microcolonies during biofilm development in both M. mediterranea and P. tunicata. LodA-mediated biofilm cell death is shown to be linked to the generation of phenotypic variation in growth and biofilm formation among M. mediterranea biofilm dispersal cells. Moreover, AlpP homologues also occur in several other gram-negative bacteria from diverse environments. Our results show that subpopulations of cells in microcolonies also die during biofilm formation in two of these organisms, Chromobacterium violaceum and Caulobacter crescentus. In all organisms, hydrogen peroxide was implicated in biofilm cell death, because it could be detected at the same time as the killing occurred, and the addition of catalase significantly reduced biofilm killing. In C. violaceum the AlpP-homologue was clearly linked to biofilm cell death events since an isogenic mutant (CVMUR1) does not undergo biofilm cell death. We propose that biofilm killing through hydrogen peroxide can be linked to AlpP homologue activity and plays an important role in dispersal and colonization across a range of gram-negative bacteria.

* Corresponding author. Mailing address: School of Biotechnology and Biomolecular Sciences and Centre for Marine 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

{triangledown} Published ahead of print on 23 May 2008.

{dagger} A.M.-P. and P.L.-E. contributed equally to this study.

Journal of Bacteriology, August 2008, p. 5493-5501, Vol. 190, No. 15
0021-9193/08/$08.00+0     doi:10.1128/JB.00549-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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