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Journal of Bacteriology, October 2001, p. 6074-6084, Vol. 183, No. 20
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.20.6074-6084.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Genetic and Physiologic Analysis of the groE Operon and Role of the HrcA Repressor in Stress Gene Regulation and Acid Tolerance in Streptococcus mutans

José A. C. Lemos,1,dagger Yi-Ywan M. Chen,1,2 and Robert A. Burne1,2,*

Center for Oral Biology1 and Department of Microbiology and Immunology,2 University of Rochester School of Medicine and Dentistry, Rochester, New York 14642

Received 21 May 2001/Accepted 24 July 2001

Our working hypothesis is that the major molecular chaperones DnaK and GroE play central roles in the ability of oral bacteria to cope with the rapid and frequent stresses encountered in oral biofilms, such as acidification and nutrient limitation. Previously, our laboratory partially characterized the dnaK operon of Streptococcus mutans (hrcA-grpE-dnaK) and demonstrated that dnaK is up-regulated in response to acid shock and sustained acidification (G. C. Jayaraman, J. E. Penders, and R. A. Burne, Mol. Microbiol. 25:329-341, 1997). Here, we show that the groESL genes of S. mutans constitute an operon that is expressed from a stress-inducible sigma A-type promoter located immediately upstream of a CIRCE element. GroEL protein and mRNA levels were elevated in cells exposed to a variety of stresses, including acid shock. A nonpolar insertion into hrcA was created and used to demonstrate that HrcA negatively regulates the expression of the groEL and dnaK operons. The SM11 mutant, which had constitutively high levels of GroESL and roughly 50% of the DnaK protein found in the wild-type strain, was more sensitive to acid killing and could not lower the pH as effectively as the parent. The acid-sensitive phenotype of SM11 was, at least in part, attributable to lower F1F0-ATPase activity. A minimum of 10 proteins, in addition to GroES-EL, were found to be up-regulated in SM11. The data clearly indicate that HrcA plays a key role in the regulation of chaperone expression in S. mutans and that changes in the levels of the chaperones profoundly influence acid tolerance.

* Corresponding author. Present address: Department of Oral Biology, P.O. Box 100424, College of Dentistry, University of Florida, Gainesville, FL 32610. Phone: (352) 392-0011. E-mail: rburne{at}dental.ufl.edu.

dagger Present address: Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL 32610.

Journal of Bacteriology, October 2001, p. 6074-6084, Vol. 183, No. 20
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.20.6074-6084.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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