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Applied and Environmental Microbiology, June 2006, p. 3916-3923, Vol. 72, No. 6
0099-2240/06/$08.00+0     doi:10.1128/AEM.03022-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Enhanced Biofilm Formation and Increased Resistance to Antimicrobial Agents and Bacterial Invasion Are Caused by Synergistic Interactions in Multispecies Biofilms{dagger}

Mette Burmølle,1 Jeremy S. Webb,2 Dhana Rao,2 Lars H. Hansen,1 Søren J. Sørensen,1 and Staffan Kjelleberg2*

Department of Microbiology, University of Copenhagen, Copenhagen, Denmark,1 School of Biotechnology and Biomolecular Sciences and Centre for Marine Biofouling and Bio-Innovation, University of New South Wales, Sydney, Australia2

Received 22 December 2005/ Accepted 20 March 2006

Most biofilms in their natural environments are likely to consist of consortia of species that influence each other in synergistic and antagonistic manners. However, few reports specifically address interactions within multispecies biofilms. In this study, 17 epiphytic bacterial strains, isolated from the surface of the marine alga Ulva australis, were screened for synergistic interactions within biofilms when present together in different combinations. Four isolates, Microbacterium phyllosphaerae, Shewanella japonica, Dokdonia donghaensis, and Acinetobacter lwoffii, were found to interact synergistically in biofilms formed in 96-well microtiter plates: biofilm biomass was observed to increase by >167% in biofilms formed by the four strains compared to biofilms composed of single strains. When exposed to the antibacterial agent hydrogen peroxide or tetracycline, the relative activity (exposed versus nonexposed biofilms) of the four-species biofilm was markedly higher than that in any of the single-species biofilms. Moreover, in biofilms established on glass surfaces in flow cells and subjected to invasion by the antibacterial protein-producing Pseudoalteromonas tunicata, the four-species biofilms resisted invasion to a greater extent than did the biofilms formed by the single species. Replacement of each strain by its cell-free culture supernatant suggested that synergy was dependent both on species-specific physical interactions between cells and on extracellular secreted factors or less specific interactions. In summary, our data strongly indicate that synergistic effects promote biofilm biomass and resistance of the biofilm to antimicrobial agents and bacterial invasion in multispecies biofilms.

* 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, Sydney, NSW 2052, Australia. Phone: 61 (2) 9385 2102. Fax: 61 (2) 9385 1779. E-mail: s.kjelleberg{at}unsw.edu.au.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, June 2006, p. 3916-3923, Vol. 72, No. 6
0099-2240/06/$08.00+0     doi:10.1128/AEM.03022-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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