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Autoinducer 2 Is Required for Biofilm Growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans

Department of Periodontics, Endodontics, and Dental Hygiene, University of Louisville School of Dentistry, Louisville, Kentucky,¹ Department of Oral Biology, University of Florida School of Dentistry, Gainesville, Florida²

Received 16 March 2007/ Returned for modification 30 April 2007/ Accepted 11 June 2007

Autoinducer 2 (AI-2) is required for the growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans in culture under conditions of iron limitation. However, in vivo this organism thrives in a complex multispecies biofilm that forms in the human oral cavity. In this report, we show that adherent growth of A. actinomycetemcomitans on a saliva-coated surface, but not planktonic growth under iron-replete conditions, is defective in a LuxS-deficient background. Biofilm growth of the luxS mutant exhibited lower total biomass and lower biofilm depth than those for the wild-type strain. Normal biofilm growth of the luxS mutant was restored genetically by introduction of a functional copy of luxS and biochemically by addition of partially purified AI-2. Furthermore, introduction of S-adenosylhomocysteine hydrolase, which restores the metabolism of S-adenosylmethionine in the absence of LuxS, into A. actinomycetemcomitans did not complement the luxS mutation unless AI-2 was added in trans. This suggests that AI-2 itself is required for biofilm growth by A. actinomycetemcomitans. A biofilm growth deficiency similar to that of the LuxS-deficient strain was also observed when a gene encoding the AI-2-interacting protein RbsB or LsrB was inactivated. Biofilm formation by A. actinomycetemcomitans was virtually eliminated upon inactivation of both rbsB and lsrB. In addition, biofilm growth by wild-type A. actinomycetemcomitans was reduced in the presence of ribose, which competes with AI-2 for binding to RbsB. These results suggest that RbsB and LsrB function as AI-2 receptors in A. actinomycetemcomitans and that the development of A. actinomycetemcomitans biofilms requires AI-2.

Published ahead of print on 25 June 2007.

Editor: F. C. Fang

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