IAI Accepts, published online ahead of print on 29 June 2009

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Infect. Immun. doi:10.1128/IAI.00345-09
Copyright (c) 2009, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Aggregatibacter actinomycetemcomitans Builds Mutualistic Biofilm Communities in Saliva With Fusobacterium nucleatum and Veillonella sp

Saravanan Periasamy and Paul E. Kolenbrander^*

Oral Infection and Immunity Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892

Human oral bacterial pathogens grow in attached multi-species biofilm communities. Unattached cells are quickly removed by swallowing. Therefore, surface attachment is essential for growth, and we investigated multi-species community interactions resulting in mutualistic growth on saliva as sole nutritional source. We used two model systems, saliva-coated transferable solid phase-polystyrene (Peg) and flowcells with saliva-coated glass surfaces. Fluorescent antibody staining and image analysis quantified biomass in flowcells: quantitative real time PCR with species-specific primers quantified biomass in Peg biofilms. Veillonella sp. PK1910, Aggregatibacter actinomycetemcomitans JP2 and Fusobacterium nucleatum ATCC 10953 were unable to grow as mono-species in flowcells. Only A. actinomycetemcomitans grew after 36 h when Pegs remained submerged in saliva from time of inoculation. Mixed-species coaggregates were used for dual- and triple-species inoculations. Biomass in dual-species biofilms increased in both systems when Veillonella sp. PK1910 was present as one of the partners. Enhanced growth of all strains was observed in triple-species biofilms in flowcells. Interestingly, in flowcells F. nucleatum and A. actinomycetemcomitans exhibited mutualism and, although F. nucleatum was unable to grow with either species in the Peg system, F. nucleatum stimulated growth of Veillonella sp. and together they enhanced the total biomass of A. actinomycetemcomitans in triple-species Peg biofilms. We propose that mutualistic dual-species and multi-species oral biofilm communities form in vivo and that mutualism between commensal veillonellae and late colonizing pathogens such as aggregatibacteria contribute to the development of periodontal disease.

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