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Journal of Bacteriology, August 2003, p. 4851-4860, Vol. 185, No. 16
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.16.4851-4860.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Autoinducer 2 Production by Streptococcus gordonii DL1 and the Biofilm Phenotype of a luxS Mutant Are Influenced by Nutritional Conditions

David S. Blehert,1 Robert J. Palmer Jr.,1 Joao B. Xavier,2 Jonas S. Almeida,3 and Paul E. Kolenbrander1*

Oral Infection and Immunity Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland 20892,1 Universidade Nova de Lisboa, Lisbon, Portugal,2 Department of Biometry and Epidemiology, Medical University of South Carolina, Charleston, South Carolina 294253

Received 5 March 2003/ Accepted 23 May 2003

The luxS gene, present in many bacterial genera, encodes the autoinducer 2 (AI-2) synthase. AI-2 has been implicated in bacterial signaling, and this study investigated its role in biofilm formation by Streptococcus gordonii, an organism that colonizes human tooth enamel within the first few hours after professional cleaning. Northern blotting and primer extension analyses revealed that S. gordonii luxS is monocistronic. AI-2 production was dependent on nutritional conditions, and maximum AI-2 induction was detected when S. gordonii was grown in the presence of serum and carbonate. In planktonic cultures, AI-2 production rose sharply during the transition from exponential to stationary phase, and the AI-2 concentration peaked approximately 4 h into stationary phase. An S. gordonii luxS mutant that did not produce AI-2 was constructed by homologous recombination. Complementation of the mutant by insertion of an intact luxS gene into the chromosome in tandem with the disrupted gene restored AI-2 production to a level similar to that of the wild-type strain. In planktonic culture, no growth differences were observed between the mutant and wild-type strains when five different media were used. However, when grown for 4 h as biofilms in 25% human saliva under flow, the luxS mutant formed tall microcolonies that differed from those formed by the wild-type and complemented mutant strains. Biofilms of the luxS mutant exhibited finger-like projections of cells that extended into the flow cell lumen. Thus, the inability to produce AI-2 is associated with altered microcolony architecture within S. gordonii biofilms formed in saliva during a time frame consistent with initial colonization of freshly cleaned enamel surfaces.

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

Journal of Bacteriology, August 2003, p. 4851-4860, Vol. 185, No. 16
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.16.4851-4860.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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