This Article Full Text 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 Ghelardi, E. Articles by Senesi, S. Search for Related Content PubMed PubMed Citation Articles by Ghelardi, E. Articles by Senesi, S.

Requirement of flhA for Swarming Differentiation, Flagellin Export, and Secretion of Virulence-Associated Proteins in Bacillus thuringiensis

Emilia Ghelardi,¹ Francesco Celandroni,¹ Sara Salvetti,¹ Douglas J. Beecher,^2, Myriam Gominet,³ Didier Lereclus,^3,4 Amy C. L. Wong,² and Sonia Senesi^1*

Dipartimento di Patologia Sperimentale, Biotecnologie Mediche, Infettivologia ed Epidemiologia, Università degli Studi di Pisa, 56127 Pisa, Italy,¹ Food Research Institute, Department of Food Microbiology and Toxicology, University of Wisconsin-Madison, Madison, Wisconsin 53706,² Unité de Biochimie Microbienne, CNRS, Institut Pasteur, 75724 Paris cedex,³ Unité de Lutte Biologique, Institut National de la Recherche Agronomique, La Miniére, Guyancourt cedex, France⁴

Received 13 June 2002/ Accepted 10 September 2002

Bacillus thuringiensis is being used worldwide as a biopesticide, although increasing evidence suggests that it is emerging as an opportunistic human pathogen. While phospholipases, hemolysins, and enterotoxins are claimed to be responsible for B. thuringiensis virulence, there is no direct evidence to indicate that the flagellum-driven motility plays a role in parasite-host interactions. This report describes the characterization of a mini-Tn10 mutant of B. thuringiensis that is defective in flagellum filament assembly and in swimming and swarming motility as well as in the production of hemolysin BL and phosphatidylcholine-preferring phospholipase C. The mutant strain was determined to carry the transposon insertion in flhA, a flagellar class II gene encoding a protein of the flagellar type III export apparatus. Interestingly, the flhA mutant of B. thuringiensis synthesized flagellin but was impaired in flagellin export. Moreover, a protein similar to the anti-sigma factor FlgM that acts in regulating flagellar class III gene transcription was not detectable in B. thuringiensis, thus suggesting that the flagellar gene expression hierarchy of B. thuringiensis differs from that described for Bacillus subtilis. The flhA mutant of B. thuringiensis was also defective in the secretion of hemolysin BL and phosphatidylcholine-preferring phospholipase C, although both of these virulence factors were synthesized by the mutant. Since complementation of the mutant with a plasmid harboring the flhA gene restored swimming and swarming motility as well as secretion of toxins, the overall results indicate that motility and virulence in B. thuringiensis may be coordinately regulated by flhA, which appears to play a crucial role in the export of flagellar as well as nonflagellar proteins.

Present address: FBI Academy, Range Rd., Quantico, VA 22135.

This article has been cited by other articles:

• 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]  
• Ghelardi, E., Celandroni, F., Salvetti, S., Ceragioli, M., Beecher, D. J., Senesi, S., Wong, A. C. L. (2007). Swarming Behavior of and Hemolysin BL Secretion by Bacillus cereus. Appl. Environ. Microbiol. 73: 4089-4093 [Abstract] [Full Text]  
• Leonard, S., Ferooz, J., Haine, V., Danese, I., Fretin, D., Tibor, A., de Walque, S., De Bolle, X., Letesson, J.-J. (2007). FtcR Is a New Master Regulator of the Flagellar System of Brucella melitensis 16M with Homologs in Rhizobiaceae. J. Bacteriol. 189: 131-141 [Abstract] [Full Text]  
• Daniels, R., Reynaert, S., Hoekstra, H., Verreth, C., Janssens, J., Braeken, K., Fauvart, M., Beullens, S., Heusdens, C., Lambrichts, I., De Vos, D. E., Vanderleyden, J., Vermant, J., Michiels, J. (2006). Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli. Proc. Natl. Acad. Sci. USA 103: 14965-14970 [Abstract] [Full Text]  
• Callegan, M. C., Novosad, B. D., Ramirez, R., Ghelardi, E., Senesi, S. (2006). Role of swarming migration in the pathogenesis of bacillus endophthalmitis.. IOVS 47: 4461-4467 [Abstract] [Full Text]  
• Bouillaut, L., Ramarao, N., Buisson, C., Gilois, N., Gohar, M., Lereclus, D., Nielsen-LeRoux, C. (2005). FlhA Influences Bacillus thuringiensis PlcR-Regulated Gene Transcription, Protein Production, and Virulence. Appl. Environ. Microbiol. 71: 8903-8910 [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]  
• Molofsky, A. B., Shetron-Rama, L. M., Swanson, M. S. (2005). Components of the Legionella pneumophila Flagellar Regulon Contribute to Multiple Virulence Traits, Including Lysosome Avoidance and Macrophage Death. Infect. Immun. 73: 5720-5734 [Abstract] [Full Text]  
• Callegan, M. C., Kane, S. T., Cochran, D. C., Novosad, B., Gilmore, M. S., Gominet, M., Lereclus, D. (2005). Bacillus Endophthalmitis: Roles of Bacterial Toxins and Motility during Infection. IOVS 46: 3233-3238 [Abstract] [Full Text]  
• Calvio, C., Celandroni, F., Ghelardi, E., Amati, G., Salvetti, S., Ceciliani, F., Galizzi, A., Senesi, S. (2005). Swarming Differentiation and Swimming Motility in Bacillus subtilis Are Controlled by swrA, a Newly Identified Dicistronic Operon. J. Bacteriol. 187: 5356-5366 [Abstract] [Full Text]  
• Arora, S. K., Neely, A. N., Blair, B., Lory, S., Ramphal, R. (2005). Role of Motility and Flagellin Glycosylation in the Pathogenesis of Pseudomonas aeruginosa Burn Wound Infections. Infect. Immun. 73: 4395-4398 [Abstract] [Full Text]  
• Fedhila, S., Guillemet, E., Nel, P., Lereclus, D. (2004). Characterization of Two Bacillus thuringiensis Genes Identified by In Vivo Screening of Virulence Factors. Appl. Environ. Microbiol. 70: 4784-4791 [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]  
• Tjalsma, H., Antelmann, H., Jongbloed, J. D.H., Braun, P. G., Darmon, E., Dorenbos, R., Dubois, J.-Y. F., Westers, H., Zanen, G., Quax, W. J., Kuipers, O. P., Bron, S., Hecker, M., van Dijl, J. M. (2004). Proteomics of Protein Secretion by Bacillus subtilis: Separating the "Secrets" of the Secretome. Microbiol. Mol. Biol. Rev. 68: 207-233 [Abstract] [Full Text]  
• Konkel, M. E., Klena, J. D., Rivera-Amill, V., Monteville, M. R., Biswas, D., Raphael, B., Mickelson, J. (2004). Secretion of Virulence Proteins from Campylobacter jejuni Is Dependent on a Functional Flagellar Export Apparatus. J. Bacteriol. 186: 3296-3303 [Abstract] [Full Text]  
• Carrillo, C. D., Taboada, E., Nash, J. H. E., Lanthier, P., Kelly, J., Lau, P. C., Verhulp, R., Mykytczuk, O., Sy, J., Findlay, W. A., Amoako, K., Gomis, S., Willson, P., Austin, J. W., Potter, A., Babiuk, L., Allan, B., Szymanski, C. M. (2004). Genome-wide Expression Analyses of Campylobacter jejuni NCTC11168 Reveals Coordinate Regulation of Motility and Virulence by flhA. J. Biol. Chem. 279: 20327-20338 [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]  
• Millikan, D. S., Ruby, E. G. (2003). FlrA, a {sigma}54-Dependent Transcriptional Activator in Vibrio fischeri, Is Required for Motility and Symbiotic Light-Organ Colonization. J. Bacteriol. 185: 3547-3557 [Abstract] [Full Text]