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Infection and Immunity, September 2009, p. 3542-3551, Vol. 77, No. 9
0019-9567/09/$08.00+0     doi:10.1128/IAI.00345-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Aggregatibacter actinomycetemcomitans Builds Mutualistic Biofilm Communities with Fusobacterium nucleatum and Veillonella Species in Saliva{triangledown}

Saravanan Periasamy and Paul E. Kolenbrander*

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

Received 25 March 2009/ Returned for modification 27 April 2009/ Accepted 18 June 2009

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

* Corresponding author. Mailing address: National Institutes of Health/NIDCR, Building 30, Room 310, 30 Convent Drive, MSC 4350, Bethesda, MD 20892-4350. Phone: (301) 496-1497. Fax: (301) 402-0396. E-mail: pkolenbrander{at}dir.nidcr.nih.gov

{triangledown} Published ahead of print on 29 June 2009.

Editor: B. A. McCormick

Infection and Immunity, September 2009, p. 3542-3551, Vol. 77, No. 9
0019-9567/09/$08.00+0     doi:10.1128/IAI.00345-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

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