This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Josenhans, C. Articles by Suerbaum, S. Search for Related Content PubMed PubMed Citation Articles by Josenhans, C. Articles by Suerbaum, S.

 Previous Article  |  Next Article 

J. Bacteriol., Jun 1995, 3010-3020, Vol 177, No. 11
Copyright © 1995, American Society for Microbiology

Comparative ultrastructural and functional studies of Helicobacter pylori and Helicobacter mustelae flagellin mutants: both flagellin subunits, FlaA and FlaB, are necessary for full motility in Helicobacter species

C Josenhans, A Labigne and S Suerbaum
Medizinische Mikrobiologie und Immunologie, Ruhr-Universitat Bochum, Germany.

Helicobacter mustelae causes chronic gastritis and ulcer disease in ferrets. It is therefore considered an important animal model of human Helicobacter pylori infection. High motility even in a viscous environment is one of the common virulence determinants of Helicobacter species. Their sheathed flagella contain a complex filament that is composed of two distinctly different flagellin subunits, FlaA and FlaB, that are coexpressed in different amounts. Here, we report the cloning and sequence determination of the flaA gene of H. mustelae NCTC12032 from a PCR amplification product. The FlaA protein has a calculated molecular mass of 53 kDa and is 73% homologous to the H. pylori FlaA subunit. Isogenic flaA and flaB mutants of H. mustelae F1 were constructed by means of reverse genetics. A method was established to generate double mutants (flaA flaB) of H. mustelae F1 as well as H. pylori N6. Genotypes, motility properties, and morphologies of the H. mustelae flagellin mutants were determined and compared with those of the H. pylori flaA and flaB mutants described previously. The flagellar organizations of the two Helicobacter species proved to be highly similar. When the flaB genes were disrupted, motility decreased by 30 to 40%. flaA mutants retained weak motility by comparison with strains that were devoid of both flagellin subunits. Weakly positive motility tests of the flaA mutants correlated with the existence of short truncated flagella. In H. mustelae, lateral as well as polar flagella were present in the truncated form. flaA flaB double mutants were completely nonmotile and lacked any form of flagella. These results show that the presence of both flagellin subunits is necessary for complete motility of Helicobacter species. The importance of this flagellar organization for the ability of the bacteria to colonize the gastric mucosa and to persist in the gastric mucus remains to be proven.

This article has been cited by other articles:

• Sterzenbach, T., Bartonickova, L., Behrens, W., Brenneke, B., Schulze, J., Kops, F., Chin, E. Y., Katzowitsch, E., Schauer, D. B., Fox, J. G., Suerbaum, S., Josenhans, C. (2008). Role of the Helicobacter hepaticus Flagellar Sigma Factor FliA in Gene Regulation and Murine Colonization. J. Bacteriol. 190: 6398-6408 [Abstract] [Full Text]  
• Li, C., Wolgemuth, C. W., Marko, M., Morgan, D. G., Charon, N. W. (2008). Genetic Analysis of Spirochete Flagellin Proteins and Their Involvement in Motility, Filament Assembly, and Flagellar Morphology. J. Bacteriol. 190: 5607-5615 [Abstract] [Full Text]  
• Schweinitzer, T., Mizote, T., Ishikawa, N., Dudnik, A., Inatsu, S., Schreiber, S., Suerbaum, S., Aizawa, S.-I., Josenhans, C. (2008). Functional Characterization and Mutagenesis of the Proposed Behavioral Sensor TlpD of Helicobacter pylori. J. Bacteriol. 190: 3244-3255 [Abstract] [Full Text]  
• Ishiyama, N., Creuzenet, C., Miller, W. L., Demendi, M., Anderson, E. M., Harauz, G., Lam, J. S., Berghuis, A. M. (2006). Structural Studies of FlaA1 from Helicobacter pylori Reveal the Mechanism for Inverting 4,6-Dehydratase Activity. J. Biol. Chem. 281: 24489-24495 [Abstract] [Full Text]  
• Kazmierczak, M. J., Wiedmann, M., Boor, K. J. (2005). Alternative Sigma Factors and Their Roles in Bacterial Virulence. Microbiol. Mol. Biol. Rev. 69: 527-543 [Abstract] [Full Text]  
• Chou, W. K., Dick, S., Wakarchuk, W. W., Tanner, M. E. (2005). Identification and Characterization of NeuB3 from Campylobacter jejuni as a Pseudaminic Acid Synthase. J. Biol. Chem. 280: 35922-35928 [Abstract] [Full Text]  
• Motaleb, M. A., Sal, M. S., Charon, N. W. (2004). The Decrease in FlaA Observed in a flaB Mutant of Borrelia burgdorferi Occurs Posttranscriptionally. J. Bacteriol. 186: 3703-3711 [Abstract] [Full Text]  
• Schultheiss, D., Kube, M., Schuler, D. (2004). Inactivation of the Flagellin Gene flaA in Magnetospirillum gryphiswaldense Results in Nonmagnetotactic Mutants Lacking Flagellar Filaments. Appl. Environ. Microbiol. 70: 3624-3631 [Abstract] [Full Text]  
• Merkx-Jacques, A., Obhi, R. K., Bethune, G., Creuzenet, C. (2004). The Helicobacter pylori flaA1 and wbpB Genes Control Lipopolysaccharide and Flagellum Synthesis and Function. J. Bacteriol. 186: 2253-2265 [Abstract] [Full Text]  
• Merrell, D. S., Thompson, L. J., Kim, C. C., Mitchell, H., Tompkins, L. S., Lee, A., Falkow, S. (2003). Growth Phase-Dependent Response of Helicobacter pylori to Iron Starvation. Infect. Immun. 71: 6510-6525 [Abstract] [Full Text]  
• Merrell, D. S., Goodrich, M. L., Otto, G., Tompkins, L. S., Falkow, S. (2003). pH-Regulated Gene Expression of the Gastric Pathogen Helicobacter pylori. Infect. Immun. 71: 3529-3539 [Abstract] [Full Text]  
• Thompson, L. J., Merrell, D. S., Neilan, B. A., Mitchell, H., Lee, A., Falkow, S. (2003). Gene Expression Profiling of Helicobacter pylori Reveals a Growth-Phase-Dependent Switch in Virulence Gene Expression. Infect. Immun. 71: 2643-2655 [Abstract] [Full Text]  
• Niehus, E., Ye, F., Suerbaum, S., Josenhans, C. (2002). Growth phase-dependent and differential transcriptional control of flagellar genes in Helicobacter pylori. Microbiology 148: 3827-3837 [Abstract] [Full Text]  
• Ottemann, K. M., Lowenthal, A. C. (2002). Helicobacter pylori Uses Motility for Initial Colonization and To Attain Robust Infection. Infect. Immun. 70: 1984-1990 [Abstract] [Full Text]  
• Martino, M. C., Stabler, R. A., Zhang, Z. W., Farthing, M. J. G., Wren, B. W., Dorrell, N. (2001). Helicobacter pylori Pore-Forming Cytolysin Orthologue TlyA Possesses In Vitro Hemolytic Activity and Has a Role in Colonization of the Gastric Mucosa. Infect. Immun. 69: 1697-1703 [Abstract] [Full Text]  
• Solnick, J. V., Schauer, D. B. (2001). Emergence of Diverse Helicobacter Species in the Pathogenesis of Gastric and Enterohepatic Diseases. Clin. Microbiol. Rev. 14: 59-97 [Abstract] [Full Text]  
• Li, C., Corum, L., Morgan, D., Rosey, E. L., Stanton, T. B., Charon, N. W. (2000). The Spirochete FlaA Periplasmic Flagellar Sheath Protein Impacts Flagellar Helicity. J. Bacteriol. 182: 6698-6706 [Abstract] [Full Text]  
• Tsutsui, N., Taneike, I., Ohara, T., Goshi, S., Kojio, S., Iwakura, N., Matsumaru, H., Wakisaka-Saito, N., Zhang, H.-M., Yamamoto, T. (2000). A Novel Action of the Proton Pump Inhibitor Rabeprazole and Its Thioether Derivative against the Motility of Helicobacter pylori. Antimicrob. Agents Chemother. 44: 3069-3073 [Abstract] [Full Text]  
• Allan, E., Dorrell, N., Foynes, S., Anyim, M., Wren, B. W. (2000). Mutational Analysis of Genes Encoding the Early Flagellar Components of Helicobacter pylori: Evidence for Transcriptional Regulation of Flagellin A Biosynthesis. J. Bacteriol. 182: 5274-5277 [Abstract] [Full Text]  
• Josenhans, C., Eaton, K. A., Thevenot, T., Suerbaum, S. (2000). Switching of Flagellar Motility in Helicobacter pylori by Reversible Length Variation of a Short Homopolymeric Sequence Repeat in fliP, a Gene Encoding a Basal Body Protein. Infect. Immun. 68: 4598-4603 [Abstract] [Full Text]  
• Clyne, M., Ocroinin, T., Suerbaum, S., Josenhans, C., Drumm, B. (2000). Adherence of Isogenic Flagellum-Negative Mutants of Helicobacter pylori and Helicobacter mustelae to Human and Ferret Gastric Epithelial Cells. Infect. Immun. 68: 4335-4339 [Abstract] [Full Text]  
• Heuner, K., Große, K., Schade, R., Göbel, U. B. (2000). A flagellar gene cluster from the oral spirochaete Treponema maltophilum. Microbiology 146: 497-507 [Abstract] [Full Text]  
• Seong Kim, J., Hoon Chang, J., Il Chung, S., Sun Yum, J. (1999). Molecular Cloning and Characterization of the Helicobacter pylori fliD Gene, an Essential Factor in Flagellar Structure and Motility. J. Bacteriol. 181: 6969-6976 [Abstract] [Full Text]  
• Marais, A., Mendz, G. L., Hazell, S. L., Megraud, F. (1999). Metabolism and Genetics of Helicobacter pylori: the Genome Era. Microbiol. Mol. Biol. Rev. 63: 642-674 [Abstract] [Full Text]  
• Porwollik, S., Noonan, B., O'Toole, P. W. (1999). Molecular Characterization of a Flagellar Export Locus of Helicobacter pylori. Infect. Immun. 67: 2060-2070 [Abstract] [Full Text]  
• Bijlsma, J. J. E., Vandenbroucke-Grauls, C. M. J. E., Phadnis, S. H., Kusters, J. G. (1999). Identification of Virulence Genes of Helicobacter pylori by Random Insertion Mutagenesis. Infect. Immun. 67: 2433-2440 [Abstract] [Full Text]  
• Spohn, G., Scarlato, V. (1999). Motility of Helicobacter pylori Is Coordinately Regulated by the Transcriptional Activator FlgR, an NtrC Homolog. J. Bacteriol. 181: 593-599 [Abstract] [Full Text]  
• Creuzenet, C., Schur, M. J., Li, J., Wakarchuk, W. W., Lam, J. S. (2000). FlaA1, a New Bifunctional UDP-GlcNAc C6 Dehydratase/ C4 Reductase from Helicobacter pylori. J. Biol. Chem. 275: 34873-34880 [Abstract] [Full Text]