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Journal of Bacteriology, July 2005, p. 4822-4829, Vol. 187, No. 14
0021-9193/05/$08.00+0     doi:10.1128/JB.187.14.4822-4829.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Analysis of the ospC Regulatory Element Controlled by the RpoN-RpoS Regulatory Pathway in Borrelia burgdorferi

Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, Texas 75390,¹ Division of Biological Sciences, The University of Montana, Missoula, Montana 59812,² Section of Rheumatology, Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520³

Received 16 February 2005/ Accepted 15 April 2005

Outer surface lipoprotein C (OspC) is a key virulence factor of Borrelia burgdorferi. ospC is differentially regulated during borrelial transmission from ticks to rodents, and such regulation is essential for maintaining the spirochete in its natural enzootic cycle. Recently, we showed that the expression of ospC in B. burgdorferi is governed by a novel alternative sigma factor regulatory network, the RpoN-RpoS pathway. However, the precise mechanism by which the RpoN-RpoS pathway controls ospC expression has been unclear. In particular, there has been uncertainty regarding whether ospC is controlled directly by RpoS (^s) or indirectly through a transactivator (induced by RpoS). Using deletion analyses and genetic complementation in an OspC-deficient mutant of B. burgdorferi, we analyzed the cis element(s) required for the expression of ospC in its native borrelial background. Two highly conserved upstream inverted repeat elements, previously implicated in ospC regulation, were not required for ospC expression in B. burgdorferi. Using similar approaches, a minimal promoter that contained a canonical –35/–10 sequence necessary and sufficient for ^s-dependent regulation of ospC was identified. Further, targeted mutagenesis of a C at position –15 within the extended –10 region of ospC, which is postulated to function like the strategic C residue important for E^s binding in Escherichia coli, abolished ospC expression. The minimal ospC promoter also was responsive to coumermycin A₁, further supporting its ^s character. The combined data constitute a body of evidence that the RpoN-RpoS regulatory network controls ospC expression by direct binding of ^s to a ^s-dependent promoter of ospC. The implication of our findings to understanding how B. burgdorferi differentially regulates ospC and other ospC-like genes via the RpoN-RpoS regulatory pathway is discussed.

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