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Journal of Bacteriology, January 2008, p. 48-60, Vol. 190, No. 1
0021-9193/08/$08.00+0     doi:10.1128/JB.01407-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Carbon Catabolite Repression of Type IV Pilus-Dependent Gliding Motility in the Anaerobic Pathogen Clostridium perfringens{triangledown} ,{dagger}

Marcelo Mendez,1,{ddagger} I-Hsiu Huang,2,3,{ddagger} Kaori Ohtani,4 Roberto Grau,1* Tohru Shimizu,4 and Mahfuzur R. Sarker2,3

Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Argentina,1 Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, Oregon,2 Department of Microbiology, College of Science, Oregon State University, Corvallis, Oregon,3 Department of Bacteriology, Kanazawa University, Kanazawa, Japan4

Received 29 August 2007/ Accepted 23 October 2007

Clostridium perfringens is an anaerobic, gram-positive, spore-forming bacterium responsible for the production of severe histotoxic and gastrointestinal diseases in humans and animals. In silico analysis of the three available genome-sequenced C. perfringens strains (13, SM101, and ATCC13124) revealed that genes that encode flagellar proteins and genes involved in chemotaxis are absent. However, those strains exhibit type IV pilus (TFP)-dependent gliding motility. Since carbon catabolite regulation has been implicated in the control of different bacterial behaviors, we investigated the effects of glucose and other readily metabolized carbohydrates on C. perfringens gliding motility. Our results demonstrate that carbon catabolite regulation constitutes an important physiological regulatory mechanism that reduces the proficiencies of the gliding motilities of a large number of unrelated human- and animal-derived pathogenic C. perfringens strains. Glucose produces a strong dose-dependent inhibition of gliding development without affecting vegetative growth. Maximum gliding inhibition was observed at a glucose concentration (1%) previously reported to also inhibit other important behaviors in C. perfringens, such as spore development. The inhibition of gliding development in the presence of glucose was due, at least in part, to the repression of the genes pilT and pilD, whose products are essential for TFP-dependent gliding proficiency. The inhibitory effects of glucose on pilT and pilD expression were under the control of the key regulatory protein CcpA (catabolite control protein A). The deficiency in CcpA activity of a ccpA knockout C. perfringens mutant strain restored the expressions of pilT and pilD and gliding proficiency in the presence of 1% glucose. The carbon catabolite repression of the gliding motility of the ccpA mutant strain was restored after the introduction of a complementing plasmid harboring a wild-type copy of ccpA. These results point to a central role for CcpA in orchestrating the negative effect of carbon catabolite regulation on C. perfringens gliding motility. Furthermore, we discovered a novel positive role for CcpA in pilT and pilD expression and gliding proficiency in the absence of catabolite regulation. Carbon catabolite repression of gliding motility and the dual role of CcpA, either as repressor or as activator of gliding, are analyzed in the context of the different social behaviors and diseases produced by C. perfringens.

* Corresponding author. Mailing address: IBR, Facultad de Bioquímica y Farmacia, Universidad Nacional de Rosario, Suipacha 531, Rosario 2000, Argentina. Phone: 54-341-4353377. Fax: 54-341-4804605. E-mail: robertograu{at}fulbrightweb.org

{triangledown} Published ahead of print on 2 November 2007.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

{ddagger} The first two authors contributed equally.

Journal of Bacteriology, January 2008, p. 48-60, Vol. 190, No. 1
0021-9193/08/$08.00+0     doi:10.1128/JB.01407-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Varga, J. J., Therit, B., Melville, S. B. (2008). Type IV Pili and the CcpA Protein Are Needed for Maximal Biofilm Formation by the Gram-Positive Anaerobic Pathogen Clostridium perfringens. Infect. Immun. 76: 4944-4951 [Abstract] [Full Text]  
  • Kinkel, T. L., McIver, K. S. (2008). CcpA-Mediated Repression of Streptolysin S Expression and Virulence in the Group A Streptococcus. Infect. Immun. 76: 3451-3463 [Abstract] [Full Text]  


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