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Infection and Immunity, September 2008, p. 3844-3853, Vol. 76, No. 9
0019-9567/08/$08.00+0     doi:10.1128/IAI.00467-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Essential Role of the Response Regulator Rrp2 in the Infectious Cycle of Borrelia burgdorferi{triangledown}

Bethany K. Boardman,1,§ Ming He,1,§ Zhiming Ouyang,2,§ Haijun Xu,1 Xiujuan Pang,3 and X. Frank Yang1*

Department of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, Indiana 46202,1 Department of Microbiology, The University of Texas Southwestern Medical Center, Dallas, Texas 75390,2 College of Pharmacy, Shenyang Pharmaceutical University, Shenyang, China3

Received 15 April 2008/ Returned for modification 27 May 2008/ Accepted 16 June 2008

Alteration of surface lipoprotein profiles is a key strategy that the Lyme disease pathogen, Borrelia burgdorferi, has evolved to be maintained within its enzootic cycle between arthropods and mammals. Accumulated evidence indicates that the central regulatory pathway controlling differential gene expression by B. burgdorferi is the RpoN-RpoS pathway (the {sigma}54-{sigma}S sigma factor cascade). It was previously shown that activation of the RpoN-RpoS pathway is controlled by Rrp2, a two-component response regulator and {sigma}54-dependent transcriptional activator. The role of Rrp2 in the infectious cycle of B. burgdorferi has not been determined heretofore. In this report, we demonstrate that an rrp2 mutant defective in activating {sigma}54-dependent transcription was unable to establish infection in mice, but the rrp2 mutant was capable of surviving within ticks during and after tick feeding. Because the rrp2 mutant was defective in the production of OspC, an outer surface lipoprotein essential for mammalian host infection, we further examined whether the loss of infectivity of the rrp2 mutant was solely due to the inability to produce OspC. While transformation with a shuttle vector carrying ospC under the control of a constitutive flaB promoter restored infection to an ospC mutant in immunodeficient SCID mice, it could not rescue the avirulent phenotype of the rrp2 mutant. These data indicate that, in addition to controlling OspC, Rrp2 controls another factor(s) essential for B. burgdorferi to establish infection in mammals. Furthermore, microarray analyses revealed that 125 and 19 genes were positively and negatively regulated, respectively, by Rrp2, which provides a foundation for future identification of additional Rrp2-dependent virulence determinants in B. burgdorferi.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, IN 46202. Phone: (317) 274-7671. Fax: (317) 274-4090. E-mail: xfyang{at}iupui.edu

{triangledown} Published ahead of print on 23 June 2008.

Editor: A. J. Bäumler

§ These authors contributed equally.

Infection and Immunity, September 2008, p. 3844-3853, Vol. 76, No. 9
0019-9567/08/$08.00+0     doi:10.1128/IAI.00467-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Blevins, J. S., Xu, H., He, M., Norgard, M. V., Reitzer, L., Yang, X. F. (2009). Rrp2, a {sigma}54-Dependent Transcriptional Activator of Borrelia burgdorferi, Activates rpoS in an Enhancer-Independent Manner. J. Bacteriol. 191: 2902-2905 [Abstract] [Full Text]  
  • Mulay, V. B., Caimano, M. J., Iyer, R., Dunham-Ems, S., Liveris, D., Petzke, M. M., Schwartz, I., Radolf, J. D. (2009). Borrelia burgdorferi bba74 Is Expressed Exclusively during Tick Feeding and Is Regulated by Both Arthropod- and Mammalian Host-Specific Signals. J. Bacteriol. 191: 2783-2794 [Abstract] [Full Text]  
  • Ouyang, Z., He, M., Oman, T., Yang, X. F., Norgard, M. V. (2009). A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 106: 3449-3454 [Abstract] [Full Text]  


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