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Infection and Immunity, December 2001, p. 7625-7634, Vol. 69, No. 12
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
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
, 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.
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