Previous Article | Next Article 
Infection and Immunity, June 2000, p. 3193-3199, Vol. 68, No. 6
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Intercellular Communication in Helicobacter
pylori: luxS Is Essential for the Production of an
Extracellular Signaling Molecule
Mark H.
Forsyth1 and
Timothy L.
Cover1,2,*
Departments of Medicine and Microbiology and
Immunology, Vanderbilt University School of
Medicine,1 and Veterans Affairs
Medical Center,2 Nashville, Tennessee
Received 13 December 1999/Returned for modification 10 February
2000/Accepted 24 February 2000
Individual bacteria of numerous species can communicate and
coordinate their actions via the production, release, and detection of
extracellular signaling molecules. In this study, we used the Vibrio harveyi luminescence bioassay to determine whether
Helicobacter pylori produces such a factor. Cell-free
conditioned media from H. pylori strains 60190 and 26695 each induced >100-fold-greater luminescence in V. harveyi
than did sterile culture medium. The H. pylori signaling
molecule had a molecular mass of <10 kDa, and its activity was
unaffected by heating to 80°C for 5 min or protease treatment. The
genome sequence of H. pylori 26695 does not contain any
gene predicted to encode an acyl homoserine lactone synthase but does
contain an orthologue of luxS, which is required for
production of autoinducer-2 (AI-2) in V. harveyi. To
evaluate the role of luxS in H. pylori, we
constructed luxS null mutants derived from H. pylori 60190 and 26695. Conditioned media from the wild-type
H. pylori strains induced >100-fold-greater luminescence in the V. harveyi bioassay than did conditioned medium from
either mutant strain. Production of the signaling molecule was restored in an H. pylori luxS null mutant strain by complementation
with a single intact copy of luxS placed in a heterologous
site on the chromosome. In addition, Escherichia coli
DH5
produced autoinducer activity following the introduction of an
intact copy of luxS from H. pylori. Production
of the signaling molecule by H. pylori was growth phase
dependent, with maximal production occurring in the mid-exponential
phase of growth. Transcription of H. pylori vacA also was
growth phase dependent, but this phenomenon was not dependent on
luxS activity. These data indicate that H. pylori produces an extracellular signaling molecule related to
AI-2 from V. harveyi. We speculate that this signaling
molecule may play a role in regulating H. pylori gene expression.
*
Corresponding author. Mailing address: Division of
Infectious Diseases, Medical Center North A3310, Vanderbilt University School of Medicine, Nashville, TN 37232-2605. Phone: (615) 322-2035. Fax: (615) 343-6160. E-mail:
covertl{at}ctrvax.vanderbilt.edu.
Infection and Immunity, June 2000, p. 3193-3199, Vol. 68, No. 6
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Williams, J. C., McInnis, K. A., Testerman, T. L.
(2008). Adherence of Helicobacter pylori to Abiotic Surfaces Is Influenced by Serum. Appl. Environ. Microbiol.
74: 1255-1258
[Abstract]
[Full Text]
-
Rader, B. A., Campagna, S. R., Semmelhack, M. F., Bassler, B. L., Guillemin, K.
(2007). The Quorum-Sensing Molecule Autoinducer 2 Regulates Motility and Flagellar Morphogenesis in Helicobacter pylori. J. Bacteriol.
189: 6109-6117
[Abstract]
[Full Text]
-
Osaki, T., Hanawa, T., Manzoku, T., Fukuda, M., Kawakami, H., Suzuki, H., Yamaguchi, H., Yan, X., Taguchi, H., Kurata, S., Kamiya, S.
(2006). Mutation of luxS affects motility and infectivity of Helicobacter pylori in gastric mucosa of a Mongolian gerbil model.. J Med Microbiol
55: 1477-1485
[Abstract]
[Full Text]
-
Lee, W.-K., Ogura, K., Loh, J. T., Cover, T. L., Berg, D. E.
(2006). Quantitative Effect of luxS Gene Inactivation on the Fitness of Helicobacter pylori. Appl. Environ. Microbiol.
72: 6615-6622
[Abstract]
[Full Text]
-
Ndagijimana, M., Vallicelli, M., Cocconcelli, P. S., Cappa, F., Patrignani, F., Lanciotti, R., Guerzoni, M. E.
(2006). Two 2[5H]-Furanones as Possible Signaling Molecules in Lactobacillus helveticus. Appl. Environ. Microbiol.
72: 6053-6061
[Abstract]
[Full Text]
-
Lombardia, E., Rovetto, A. J., Arabolaza, A. L., Grau, R. R.
(2006). A LuxS-Dependent Cell-to-Cell Language Regulates Social Behavior and Development in Bacillus subtilis.. J. Bacteriol.
188: 4442-4452
[Abstract]
[Full Text]
-
Hamblin, M. R., Viveiros, J., Yang, C., Ahmadi, A., Ganz, R. A., Tolkoff, M. J.
(2005). Helicobacter pylori Accumulates Photoactive Porphyrins and Is Killed by Visible Light. Antimicrob. Agents Chemother.
49: 2822-2827
[Abstract]
[Full Text]
-
Loh, J. T., Forsyth, M. H., Cover, T. L.
(2004). Growth Phase Regulation of flaA Expression in Helicobacter pylori Is luxS Dependent. Infect. Immun.
72: 5506-5510
[Abstract]
[Full Text]
-
Jones, M. B., Blaser, M. J.
(2003). Detection of a luxS-Signaling Molecule in Bacillus anthracis. Infect. Immun.
71: 3914-3919
[Abstract]
[Full Text]
-
Dove, J. E., Yasukawa, K., Tinsley, C. R., Nassif, X.
(2003). Production of the signalling molecule, autoinducer-2, by Neisseria meningitidis: lack of evidence for a concerted transcriptional response. Microbiology
149: 1859-1869
[Abstract]
[Full Text]
-
Merritt, J., Qi, F., Goodman, S. D., Anderson, M. H., Shi, W.
(2003). Mutation of luxS Affects Biofilm Formation in Streptococcus mutans. Infect. Immun.
71: 1972-1979
[Abstract]
[Full Text]
-
Hardie, K. R., Cooksley, C., Green, A. D., Winzer, K.
(2003). Autoinducer 2 activity in Escherichia coli culture supernatants can be actively reduced despite maintenance of an active synthase, LuxS. Microbiology
149: 715-728
[Abstract]
[Full Text]
-
McNab, R., Ford, S. K., El-Sabaeny, A., Barbieri, B., Cook, G. S., Lamont, R. J.
(2003). LuxS-Based Signaling in Streptococcus gordonii: Autoinducer 2 Controls Carbohydrate Metabolism and Biofilm Formation with Porphyromonas gingivalis. J. Bacteriol.
185: 274-284
[Abstract]
[Full Text]
-
Cloak, O. M., Solow, B. T., Briggs, C. E., Chen, C.-Y., Fratamico, P. M.
(2002). Quorum Sensing and Production of Autoinducer-2 in Campylobacter spp., Escherichia coli O157:H7, and Salmonella enterica Serovar Typhimurium in Foods. Appl. Environ. Microbiol.
68: 4666-4671
[Abstract]
[Full Text]
-
Forsyth, M. H., Cao, P., Garcia, P. P., Hall, J. D., Cover, T. L.
(2002). Genome-Wide Transcriptional Profiling in a Histidine Kinase Mutant of Helicobacter pylori Identifies Members of a Regulon. J. Bacteriol.
184: 4630-4635
[Abstract]
[Full Text]
-
Beeston, A. L., Surette, M. G.
(2002). pfs-Dependent Regulation of Autoinducer 2 Production in Salmonella enterica Serovar Typhimurium. J. Bacteriol.
184: 3450-3456
[Abstract]
[Full Text]
-
Elvers, K. T., Park, S. F.
(2002). Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology
148: 1475-1481
[Abstract]
[Full Text]
-
Winzer, K., Sun, Y.-h., Green, A., Delory, M., Blackley, D., Hardie, K. R., Baldwin, T. J., Tang, C. M.
(2002). Role of Neisseria meningitidis luxS in Cell-to-Cell Signaling and Bacteremic Infection. Infect. Immun.
70: 2245-2248
[Abstract]
[Full Text]
-
Winzer, K., Hardie, K. R., Burgess, N., Doherty, N., Kirke, D., Holden, M. T. G., Linforth, R., Cornell, K. A., Taylor, A. J., Hill, P. J., Williams, P.
(2002). LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology
148: 909-922
[Abstract]
[Full Text]
-
Burgess, N. A., Kirke, D. F., Williams, P., Winzer, K., Hardie, K. R., Meyers, N. L., Aduse-Opoku, J., Curtis, M. A., Camara, M.
(2002). LuxS-dependent quorum sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence. Microbiology
148: 763-772
[Abstract]
[Full Text]
-
Schneider, R., Lockatell, C. V., Johnson, D., Belas, R.
(2002). Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology
148: 773-782
[Abstract]
[Full Text]
-
Hilgers, M. T., Ludwig, M. L.
(2001). Crystal structure of the quorum-sensing protein LuxS reveals a catalytic metal site. Proc. Natl. Acad. Sci. USA
10.1073/pnas.191223098v1
[Abstract]
[Full Text]
-
Rokbi, B., Seguin, D., Guy, B., Mazarin, V., Vidor, E., Mion, F., Cadoz, M., Quentin-Millet, M.-J.
(2001). Assessment of Helicobacter pylori Gene Expression within Mouse and Human Gastric Mucosae by Real-Time Reverse Transcriptase PCR. Infect. Immun.
69: 4759-4766
[Abstract]
[Full Text]
-
Chung, W. O., Park, Y., Lamont, R. J., McNab, R., Barbieri, B., Demuth, D. R.
(2001). Signaling System in Porphyromonas gingivalis Based on a LuxS Protein. J. Bacteriol.
183: 3903-3909
[Abstract]
[Full Text]
-
Frias, J., Olle, E., Alsina, M.
(2001). Periodontal Pathogens Produce Quorum Sensing Signal Molecules. Infect. Immun.
69: 3431-3434
[Abstract]
[Full Text]
-
Hilgers, M. T., Ludwig, M. L.
(2001). Crystal structure of the quorum-sensing protein LuxS reveals a catalytic metal site. Proc. Natl. Acad. Sci. USA
98: 11169-11174
[Abstract]
[Full Text]