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Infection and Immunity, December 2001, p. 7625-7634, Vol. 69, No. 12
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.12.7625-7634.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Intra- and Interspecies Regulation of Gene Expression by Actinobacillus actinomycetemcomitans LuxS

Karen P. Fong,1 Whasun O. Chung,2 Richard J. Lamont,2 and Donald R. Demuth1,*

Department of Biochemistry, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania,1 and Department of Oral Biology, University of Washington, Seattle, Washington2

Received 6 July 2001/Returned for modification 28 August 2001/Accepted 17 September 2001

The cell density-dependent control of gene expression is employed by many bacteria for regulating a variety of physiological functions, including the generation of bioluminescence, sporulation, formation of biofilms, and the expression of virulence factors. Although periodontal organisms do not appear to secrete acyl-homoserine lactone signals, several species, e.g., Porphyromonas gingivalis, Prevotella intermedia, and Fusobacterium nucleatum, have recently been shown to secrete a signal related to the autoinducer II (AI-2) of the signal system 2 pathway in Vibrio harveyi. Here, we report that the periodontal pathogen Actinobacillus actinomycetemcomitans expresses a homolog of V. harveyi luxS and secretes an AI-2-like signal. Cell-free conditioned medium from A. actinomycetemcomitans or from a recombinant Escherichia coli strain (E. coli AIS) expressing A. actinomycetemcomitans luxS induced luminescence in V. harveyi BB170 >200-fold over controls. AI-2 levels peaked in mid-exponential-phase cultures of A. actinomycetemcomitans and were significantly reduced in late-log- and stationary-phase cultures. Incubation of early-log-phase A. actinomycetemcomitans cells with conditioned medium from A. actinomycetemcomitans or from E. coli AIS resulted in a threefold induction of leukotoxic activity and a concomitant increase in leukotoxin polypeptide. In contrast, no increase in leukotoxin expression occurred when cells were exposed to sterile medium or to conditioned broth from E. coli AIS-, a recombinant strain in which luxS was insertionally inactivated. A. actinomycetemcomitans AI-2 also induced expression of afuA, encoding a periplasmic iron transport protein, approximately eightfold, suggesting that LuxS-dependent signaling may play a role in the regulation of iron acquisition by A. actinomycetemcomitans. Finally, A. actinomycetemcomitans AI-2 added in trans complemented a luxS knockout mutation in P. gingivalis by modulating the expression of the luxS-regulated genes uvrB and hasF in this organism. Together, these results suggest that LuxS-dependent signaling may modulate aspects of virulence and the uptake of iron by A. actinomycetemcomitans and induce responses in other periodontal organisms in mixed-species oral biofilm.

* Corresponding author. Mailing address: Room 540, Levy Research Building, Department of Biochemistry, School of Dental Medicine, University of Pennsylvania, 4010 Locust St., Philadelphia, PA 19014-6002. Phone: (215) 898-2125. Fax: (215) 898-3695. E-mail: demuth{at}biochem.dental.upenn.edu.

Infection and Immunity, December 2001, p. 7625-7634, Vol. 69, No. 12
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.12.7625-7634.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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