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Journal of Bacteriology, January 2003, p. 274-284, Vol. 185, No. 1
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.1.274-284.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

LuxS-Based Signaling in Streptococcus gordonii: Autoinducer 2 Controls Carbohydrate Metabolism and Biofilm Formation with Porphyromonas gingivalis

Roderick McNab,1* Suzannah K. Ford,1 Azza El-Sabaeny,2 Bruno Barbieri,1 Guy S. Cook,3 and Richard J. Lamont2,{dagger}

Department of Microbiology, Eastman Dental Institute, University College, London WC1 8LD, United Kingdom,1 Department of Oral Biology, University of Washington, Seattle, Washington 98195,2 Bacterin, Inc., Bozeman, Montana 597153

Received 31 July 2002/ Accepted 7 October 2002

Communication based on autoinducer 2 (AI-2) is widespread among gram-negative and gram-positive bacteria, and the AI-2 pathway can control the expression of genes involved in a variety of metabolic pathways and pathogenic mechanisms. In the present study, we identified luxS, a gene responsible for the synthesis of AI-2, in Streptococcus gordonii, a major component of the dental plaque biofilm. S. gordonii conditioned medium induced bioluminescence in an AI-2 reporter strain of Vibrio harveyi. An isogenic mutant of S. gordonii, generated by insertional inactivation of the luxS gene, was unaffected in growth and in its ability to form biofilms on polystyrene surfaces. In contrast, the mutant strain failed to induce bioluminescence in V. harveyi and was unable to form a mixed species biofilm with a LuxS-null strain of the periodontal pathogen Porphyromonas gingivalis. Complementation of the luxS mutation in S. gordonii restored normal biofilm formation with the luxS-deficient P. gingivalis. Differential display PCR demonstrated that the inactivation of S. gordonii luxS downregulated the expression of a number of genes, including gtfG, encoding glucosyltransferase; fruA, encoding extracellular exo-ß-D-fructosidase; and lacD encoding tagatose 1,6-diphosphate aldolase. However, S. gordonii cell surface expression of SspA and SspB proteins, previously implicated in mediating adhesion between S. gordonii and P. gingivalis, was unaffected by inactivation of luxS. The results suggest that S. gordonii produces an AI-2-like signaling molecule that regulates aspects of carbohydrate metabolism in the organism. Furthermore, LuxS-dependent intercellular communication is essential for biofilm formation between nongrowing cells of P. gingivalis and S. gordonii.

* Corresponding author. Mailing address: GlaxoSmithKline Consumer Healthcare, St. George's Ave., Weybridge, Surrey KT13 0DE, United Kingdom. Phone: 44(0)1932-822257. Fax: 44(0)1932-822120. E-mail: rod.x.mcnab{at}gsk.com.

{dagger} Present address: Department of Oral Biology, University of Florida, Gainesville, FL 32610.

Journal of Bacteriology, January 2003, p. 274-284, Vol. 185, No. 1
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.1.274-284.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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