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Infection and Immunity, April 2002, p. 2245-2248, Vol. 70, No. 4
0019-9567/02/$04.00+0 DOI: 10.1128/IAI.70.4.2245-2248.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
Role of Neisseria meningitidis luxS in Cell-to-Cell Signaling and Bacteremic Infection
Klaus Winzer,1 Yao-hui Sun,2 Andrew Green,1 Marie Delory,2 David Blackley,1 Kim R. Hardie,1 Thomas J. Baldwin,1 and Christoph M. Tang3*
Institute of Infections and Immunity, Queen's Medical Centre, Nottingham NG9 2EX,1
Department of Infectious Diseases, Centre for Molecular Microbiology and Infection, Imperial College of Technology, Science, and Medicine, London SW7 2AZ,3
Department of Paediatrics, John Radcliffe Hospital, Headington, Oxford OX3 9DU, United Kingdom2
Received 17 September 2001/
Returned for modification 5 November 2001/
Accepted 15 January 2002

ABSTRACT
Numerous pathogenic bacteria contain
luxS, which is required
for autoinducer-2 production. Here, we demonstrate that
Neisseria meningitidis contains a functional copy of
luxS that is necessary
for full meningococcal virulence; strains with a
luxS deletion
are defective for bacteremia, a prerequisite of meningococcal
pathogenesis.

TEXT
Bacteria have evolved mechanisms to coordinate gene expression
in response to population density. Known as quorum sensing,
these mechanisms involve the production and detection of signaling
molecules (called autoinducers or pheromones), which modulate
critical functions including virulence factor production, plasmid
conjugal transfer, activation of secretion systems, swarming,
swimming and twitching motility, biofilm differentiation, and
bioluminescence (for reviews, see references
2,
13,
15,
28,
and
30). Thus, bacteria in populations display properties denied
individual cells.
Gram-positive and gram-negative bacteria are known to utilize distinct signal molecules for quorum sensing. Gram-positive bacteria export and detect small peptides, while gram-negative bacteria produce membrane-permeative N-acyl homoserine lactones (13, 15). Recently, however, potential quorum sensing systems based on a signal molecule called autoinducer-2 (AI-2) were shown to be present in both gram-positive and gram-negative species (2, 23, 24). The luxS gene product is required for AI-2 production by Salmonella enterica serovar Typhimurium (24), Escherichia coli (19, 23), Shigella flexneri (6), Helicobacter pylori (9, 11), Porphyromonas gingivalis (4, 5), Streptococcus pyogenes (12), and Actinobacillus actinomycetemcomitans (8). The chemical structure of AI-2 appears to be conserved, possibly allowing interspecies communication (2, 3, 18).
Neisseria meningitidis colonizes the human nasopharynx and can cause meningitis and/or septicemia (16). Here, we demonstrate that N. meningitidis possesses a functional luxS necessary for AI-2 production and full meningococcal virulence.
Serogroup B N. meningitidis possesses a functional luxS gene.
Investigation of the MC58 genome sequence (25) using LuxS from Vibrio harveyi (LuxSVh) led to the identification of NMB1981 (N. meningitidis serogroup B annotated sequence), a 504-bp open reading frame (ORF) with 80% identity to LuxSVh which is annotated as being of unknown function. To establish whether NMB1981 encodes a functional product, the gene was amplified with rTth DNA polymerase XL (Perkin-Elmer, Warrington, United Kingdom), ligated in both orientations into pGEM T-Easy (Promega, Madison, Wis.), and then transferred into Escherichia coli DH5
, which cannot produce AI-2 due to a mutation in luxS (24). Strains were grown at 37°C in Luria-Bertani medium, and AI-2 production was assayed using V. harveyi BB170 as the reporter (3). Exogenous AI-2 induces premature bioluminescence by this reporter strain. Only clones containing NMB1981 expressed through the vector-encoded promoter (pGEMluxS-F) produced culture supernatants with AI-2 activity (Fig. 1A); no activity was detected if the insert was in the opposite orientation (pGEMluxS-R). Identical results were obtained with the NMB1981 homologue from strain SD (data not shown). Thus, NMB1981 complements the defective luxS in DH5
and was designated luxSNm.
Expression of N. meningitidis AI-2 activity is dependent on luxSNm.
Next, we investigated whether
N. meningitidis initiates
luxSNm-dependent
AI-2 production. A total of 432 bp of
luxSNm (nucleotides 4
to 436 of the ORF) was deleted by inverse PCR and replaced with
the kanamycin resistance gene from Tn
903, yielding pGEM
luxS-kan.
The insert of pGEM
luxS-kan was then cloned into pGIT5.3, a vector
containing the
Neisseria uptake sequence, and the resulting
plasmid (pGIT5.3
luxS-kan) was introduced into
N. meningitidis by transformation; Southern hybridization confirmed the integration
of the deleted allele in MC58
luxS and B16/B6
luxS. A complemented
strain, MC58
luxSEct, was constructed to enable the attribution
of functions to
luxSNm.
luxSNm, under the control of an
opa promoter, was introduced in the intergenic region between NMB102
and NMB103 (genes oriented in a tail-to-tail fashion), with
ermC downstream of
luxS. The construct (pYH204) was introduced
into MC58
luxS by transformation, generating MC58
luxSEct; Southern
analysis confirmed that integration into the NMB102/NMB103 intergenic
region had occurred.
N. meningitidis bacteria were grown at
37°C on brain heart infusion plates with Levinthal's supplement
or in Mueller-Hinton medium for 24 h with shaking for AI-2 production.
A list of the bacterial strains and plasmids used in this study
is presented in Table
1.
AI-2 activity was detected in MC58 culture supernatants from
early logarithmic growth onward (Fig.
1B). While no AI-2 activity
was observed in supernatants of MC58
luxS, the single ectopic
luxS allele in MC58
luxSEct restored AI-2 activity to wild-type
levels. Identical results were obtained with strain B16/B6 and
its corresponding mutants (not shown).
N. meningitidis luxS mutants are attenuated for bacteremic infection.
To investigate the influence of luxSNm on meningococcal pathogenesis, the ability of MC58
luxS to cause disseminated disease was compared directly against that of MC58. Bacteria were grown overnight on brain heart infusion agar and suspended in phosphate-buffered saline, and the number of CFU was determined. Bacteria (100 µl) in phosphate-buffered saline were injected intraperitoneally into five-day-old infant rats (Wistar; Harlan, Bicester, United Kingdom). The virulence of strains was assessed using groups of at least three animals in each of three experiments by determining their competitive index (CI). The CI is the proportion of mutant to wild-type bacteria recovered from the bloodstream following inoculation with a 1:1 ratio of the strains (26); results were compared by using a one-tailed Student's t test. MC58
luxS showed decreased survival in infected animals when compared with MC58 (P < 0.01; Fig. 2). Similar results were obtained with B16/B6 (not shown). Providing luxSNm in trans (MC58
luxSEct) restored the virulence to wild-type levels, demonstrating that the loss of luxS, not any polar effect, is responsible for attenuation.
Complete genome sequences of bacterial pathogens provide an
important resource for microbial research (
21), though the annotations
may miss biologically important homologies. While a
luxS homologue
was identified in the annotated Z2491 serogroup A strain sequence
(
14), the annotated MC58 genome (
25) does not contain a
luxS homologue. However, investigation of the MC58 database revealed
an ORF closely related to
luxSVh. We demonstrate that
luxSNm complements DH5

and that
N. meningitidis expresses AI-2 in a
luxS-dependent fashion with maximal production during late exponential
growth, consistent with a role in quorum sensing.
Studies with the infant rat model show that luxSNm contributes to the ability of the bacterium to cause bacteremia, a prerequisite for meningococcal pathogenicity. This model has been used to demonstrate the influence of other well-characterized virulence determinants on disseminated infection (20, 27). Although CIs provide a sensitive measure of a strain's virulence by eliminating host-to-host variation (22, 26), our findings may underestimate the impact of luxSNm on pathogenesis. AI-2 produced by the wild type could partially cross-feed a luxSNm mutant in mixed-inoculum experiments. However, the results are also consistent with a metabolic function of the LuxS protein, which is distinct from quorum sensing (18, 29).
Little is known about the regulatory networks governing the expression of N. meningitidis virulence factors apart from that of a LysR homologue, required for entry into host cells (7). Identification of the response elements and the genes controlled by AI-2-dependent signaling may help elucidate this aspect of pathogenesis and identify novel virulence determinants for this important human pathogen. Furthermore, the demonstration that luxSNm is required for full virulence suggests that interrupting this pathway may provide a means for preventing meningococcal disease (10).

ACKNOWLEDGMENTS
We are grateful to Sharmila Bakshi, David Holden, Harry Smith,
Nick West, and Paul Williams for valuable comments during preparation
of the manuscript.
C.M.T. is an MRC Clinician Scientist, and A.G. was supported by a studentship from the University of Nottingham. Work in C.M.T.'s laboratory is supported by the Meningitis Research Fund. K.W. is supported by the MRC, and K.H. is a British Society for Antimicrobial Chemotherapy Fellow.

FOOTNOTES
* Corresponding author. Mailing address: Department of Infectious Diseases, Center for Molecular Microbiology and Infection, Flowers Building, Imperial College of Technology, Science, and Medicine, Armstrong Rd., London SW7 2AZ, United Kingdom. Phone: (44) 207-594-3072. Fax: (44) 207-594-3076. E-mail:
c.tang{at}ic.ac.uk.

Editor: V. J. DiRita

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Infection and Immunity, April 2002, p. 2245-2248, Vol. 70, No. 4
0019-9567/02/$04.00+0 DOI: 10.1128/IAI.70.4.2245-2248.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
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