This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Young, G. M.
Right arrow Articles by Miller, V. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Young, G. M.
Right arrow Articles by Miller, V. L.

 Previous Article  |  Next Article 

Journal of Bacteriology, May 1999, p. 2823-2833, Vol. 181, No. 9
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

The Yersinia enterocolitica Motility Master Regulatory Operon, flhDC, Is Required for Flagellin Production, Swimming Motility, and Swarming Motility

Glenn M. Young,1 Michael J. Smith,2 Scott A. Minnich,2 and Virginia L. Miller1,3,*

Departments of Molecular Microbiology1 and Pediatrics,3 Washington University School of Medicine, St. Louis, Missouri 63110, and Department of Microbiology, Molecular Biology and Biochemistry, University of Idaho, Moscow, Idaho 838432

Received 18 November 1998/Accepted 16 February 1999

The ability to move over and colonize surface substrata has been linked to the formation of biofilms and to the virulence of some bacterial pathogens. Results from this study show that the gastrointestinal pathogen Yersinia enterocolitica can migrate over and colonize surfaces by swarming motility, a form of cooperative multicellular behavior. Immunoblot analysis and electron microscopy indicated that swarming motility is dependent on the same flagellum organelle that is required for swimming motility, which occurs in fluid environments. Furthermore, motility genes such as flgEF, flgMN, flhBA, and fliA, known to be required for the production of flagella, are essential for swarming motility. To begin to investigate how environmental signals are processed and integrated by Y. enterocolitica to stimulate the production of flagella and regulate these two forms of cell migration, the motility master regulatory operon, flhDC, was cloned. Mutations within flhDC completely abolished swimming motility, swarming motility, and flagellin production. DNA sequence analysis revealed that this locus is similar to motility master regulatory operons of other gram-negative bacteria. Genetic complementation and functional analysis of flhDC indicated that it is required for the production of flagella. When flhDC was expressed from an inducible ptac promoter, flagellin production was shown to be dependent on levels of flhDC expression. Phenotypically, induction of the ptac-flhDC fusion also corresponded to increased levels of both swimming and swarming motility.

* Corresponding author. Mailing address: Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110. Phone: (314) 747-2132. Fax: (314) 747-2135. E-mail: virginia{at}borcim.wustl.edu.

Journal of Bacteriology, May 1999, p. 2823-2833, Vol. 181, No. 9
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Hu, Y., Wang, Y., Ding, L., Lu, P., Atkinson, S., Chen, S. (2009). Positive regulation of flhDC expression by OmpR in Yersinia pseudotuberculosis. Microbiology 155: 3622-3631 [Abstract] [Full Text]  
  • Salvetti, S., Celandroni, F., Ceragioli, M., Senesi, S., Ghelardi, E. (2009). Identification of non-flagellar genes involved in swarm cell differentiation using a Bacillus thuringiensis mini-Tn10 mutant library. Microbiology 155: 912-921 [Abstract] [Full Text]  
  • Axler-DiPerte, G. L., Hinchliffe, S. J., Wren, B. W., Darwin, A. J. (2009). YtxR Acts as an Overriding Transcriptional Off Switch for the Yersinia enterocolitica Ysc-Yop Type 3 Secretion System. J. Bacteriol. 191: 514-524 [Abstract] [Full Text]  
  • Kim, T.-J., Young, B. M., Young, G. M. (2008). Effect of Flagellar Mutations on Yersinia enterocolitica Biofilm Formation. Appl. Environ. Microbiol. 74: 5466-5474 [Abstract] [Full Text]  
  • Hatt, J. K., Rather, P. N. (2008). Characterization of a Novel Gene, wosA, Regulating FlhDC Expression in Proteus mirabilis. J. Bacteriol. 190: 1946-1955 [Abstract] [Full Text]  
  • Claret, L., Miquel, S., Vieille, N., Ryjenkov, D. A., Gomelsky, M., Darfeuille-Michaud, A. (2007). The Flagellar Sigma Factor FliA Regulates Adhesion and Invasion of Crohn Disease-associated Escherichia coli via a Cyclic Dimeric GMP-dependent Pathway. J. Biol. Chem. 282: 33275-33283 [Abstract] [Full Text]  
  • Falker, S., Schilling, J., Schmidt, M. A., Heusipp, G. (2007). Overproduction of DNA Adenine Methyltransferase Alters Motility, Invasion, and the Lipopolysaccharide O-Antigen Composition of Yersinia enterocolitica. Infect. Immun. 75: 4990-4997 [Abstract] [Full Text]  
  • Salvetti, S., Ghelardi, E., Celandroni, F., Ceragioli, M., Giannessi, F., Senesi, S. (2007). FlhF, a signal recognition particle-like GTPase, is involved in the regulation of flagellar arrangement, motility behaviour and protein secretion in Bacillus cereus. Microbiology 153: 2541-2552 [Abstract] [Full Text]  
  • McNally, A., La Ragione, R. M., Best, A., Manning, G., Newell, D. G. (2007). An aflagellate mutant Yersinia enterocolitica biotype 1A strain displays altered invasion of epithelial cells, persistence in macrophages, and cytokine secretion profiles in vitro. Microbiology 153: 1339-1349 [Abstract] [Full Text]  
  • Perez-Gutierrez, C., Llompart, C. M., Skurnik, M., Bengoechea, J. A. (2007). Expression of the Yersinia enterocolitica pYV-Encoded Type III Secretion System Is Modulated by Lipopolysaccharide O-Antigen Status. Infect. Immun. 75: 1512-1516 [Abstract] [Full Text]  
  • Atkinson, S., Chang, C.-Y., Sockett, R. E., Camara, M., Williams, P. (2006). Quorum Sensing in Yersinia enterocolitica Controls Swimming and Swarming Motility. J. Bacteriol. 188: 1451-1461 [Abstract] [Full Text]  
  • Belas, R., Suvanasuthi, R. (2005). The Ability of Proteus mirabilis To Sense Surfaces and Regulate Virulence Gene Expression Involves FliL, a Flagellar Basal Body Protein. J. Bacteriol. 187: 6789-6803 [Abstract] [Full Text]  
  • Bigot, A., Pagniez, H., Botton, E., Frehel, C., Dubail, I., Jacquet, C., Charbit, A., Raynaud, C. (2005). Role of FliF and FliI of Listeria monocytogenes in Flagellar Assembly and Pathogenicity. Infect. Immun. 73: 5530-5539 [Abstract] [Full Text]  
  • Stafford, G. P., Ogi, T., Hughes, C. (2005). Binding and transcriptional activation of non-flagellar genes by the Escherichia coli flagellar master regulator FlhD2C2. Microbiology 151: 1779-1788 [Abstract] [Full Text]  
  • Bindel Connelly, M., Young, G. M., Sloma, A. (2004). Extracellular Proteolytic Activity Plays a Central Role in Swarming Motility in Bacillus subtilis. J. Bacteriol. 186: 4159-4167 [Abstract] [Full Text]  
  • Millikan, D. S., Ruby, E. G. (2004). Vibrio fischeri Flagellin A Is Essential for Normal Motility and for Symbiotic Competence during Initial Squid Light Organ Colonization. J. Bacteriol. 186: 4315-4325 [Abstract] [Full Text]  
  • Kapatral, V., Campbell, J. W., Minnich, S. A., Thomson, N. R., Matsumura, P., Pruss, B. M. (2004). Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 150: 2289-2300 [Abstract] [Full Text]  
  • Monday, S. R., Minnich, S. A., Feng, P. C. H. (2004). A 12-Base-Pair Deletion in the Flagellar Master Control Gene flhC Causes Nonmotility of the Pathogenic German Sorbitol-Fermenting Escherichia coli O157:H- Strains. J. Bacteriol. 186: 2319-2327 [Abstract] [Full Text]  
  • Senesi, S., Ghelardi, E., Celandroni, F., Salvetti, S., Parisio, E., Galizzi, A. (2004). Surface-Associated Flagellum Formation and Swarming Differentiation in Bacillus subtilis Are Controlled by the ifm Locus. J. Bacteriol. 186: 1158-1164 [Abstract] [Full Text]  
  • DeBord, K. L., Galanopoulos, N. S., Schneewind, O. (2003). The ttsA Gene Is Required for Low-Calcium-Induced Type III Secretion of Yop Proteins and Virulence of Yersinia enterocolitica W22703. J. Bacteriol. 185: 3499-3507 [Abstract] [Full Text]  
  • Ghelardi, E., Celandroni, F., Salvetti, S., Beecher, D. J., Gominet, M., Lereclus, D., Wong, A. C. L., Senesi, S. (2002). Requirement of flhA for Swarming Differentiation, Flagellin Export, and Secretion of Virulence-Associated Proteins in Bacillus thuringiensis. J. Bacteriol. 184: 6424-6433 [Abstract] [Full Text]  
  • Morohoshi, T., Maruo, T., Shirai, Y., Kato, J., Ikeda, T., Takiguchi, N., Ohtake, H., Kuroda, A. (2002). Accumulation of Inorganic Polyphosphate in phoU Mutants of Escherichia coli and Synechocystis sp. Strain PCC6803. Appl. Environ. Microbiol. 68: 4107-4110 [Abstract] [Full Text]  
  • Petersen, S., Young, G. M. (2002). Essential Role for Cyclic AMP and Its Receptor Protein in Yersinia enterocolitica Virulence. Infect. Immun. 70: 3665-3672 [Abstract] [Full Text]  
  • Bleves, S., Marenne, M.-N., Detry, G., Cornelis, G. R. (2002). Up-Regulation of the Yersinia enterocolitica yop Regulon by Deletion of the Flagellum Master Operon flhDC. J. Bacteriol. 184: 3214-3223 [Abstract] [Full Text]  
  • Senesi, S., Celandroni, F., Salvetti, S., Beecher, D. J., Wong, A. C. L., Ghelardi, E. (2002). Swarming motility in Bacillus cereus and characterization of a fliY mutant impaired in swarm cell differentiation. Microbiology 148: 1785-1794 [Abstract] [Full Text]  
  • Schembri, M. A., Givskov, M., Klemm, P. (2002). An Attractive Surface: Gram-Negative Bacterial Biofilms. Sci Signal 2002: re6-re6 [Abstract] [Full Text]  
  • Young, B. M., Young, G. M. (2002). YplA Is Exported by the Ysc, Ysa, and Flagellar Type III Secretion Systems of Yersinia enterocolitica. J. Bacteriol. 184: 1324-1334 [Abstract] [Full Text]  
  • Kirov, S. M., Tassell, B. C., Semmler, A. B. T., O'Donovan, L. A., Rabaan, A. A., Shaw, J. G. (2002). Lateral Flagella and Swarming Motility in Aeromonas Species. J. Bacteriol. 184: 547-555 [Abstract] [Full Text]  
  • Nelson, K. M., Young, G. M., Miller, V. L. (2001). Identification of a Locus Involved in Systemic Dissemination of Yersinia enterocolitica. Infect. Immun. 69: 6201-6208 [Abstract] [Full Text]  
  • Laguna, R., Romo, J., Read, B. A., Wahlund, T. M. (2001). Induction of Phase Variation Events in the Life Cycle of the Marine Coccolithophorid Emiliania huxleyi. Appl. Environ. Microbiol. 67: 3824-3831 [Abstract] [Full Text]  
  • Brown, I. I., Häse, C. C. (2001). Flagellum-Independent Surface Migration of Vibrio cholerae and Escherichia coli. J. Bacteriol. 183: 3784-3790 [Abstract] [Full Text]  
  • Badger, J. L., Young, B. M., Darwin, A. J., Miller, V. L. (2000). Yersinia enterocolitica ClpB Affects Levels of Invasin and Motility. J. Bacteriol. 182: 5563-5571 [Abstract] [Full Text]  
  • Young, G. M., Badger, J. L., Miller, V. L. (2000). Motility Is Required To Initiate Host Cell Invasion by Yersinia enterocolitica. Infect. Immun. 68: 4323-4326 [Abstract] [Full Text]  
  • Schmiel, D. H., Young, G. M., Miller, V. L. (2000). The Yersinia enterocolitica Phospholipase Gene yplA Is Part of the Flagellar Regulon. J. Bacteriol. 182: 2314-2320 [Abstract] [Full Text]  
  • Givaudan, A., Lanois, A. (2000). flhDC, the Flagellar Master Operon of Xenorhabdus nematophilus: Requirement for Motility, Lipolysis, Extracellular Hemolysis, and Full Virulence in Insects. J. Bacteriol. 182: 107-115 [Abstract] [Full Text]  
  • Rashid, M. H., Kornberg, A. (2000). Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 97: 4885-4890 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»