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Journal of Bacteriology, July 2005, p. 4488-4496, Vol. 187, No. 13
0021-9193/05/$08.00+0     doi:10.1128/JB.187.13.4488-4496.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Staphylococcus aureus ClpC Is Required for Stress Resistance, Aconitase Activity, Growth Recovery, and Death

Indranil Chatterjee,1 Petra Becker,2 Matthias Grundmeier,2 Markus Bischoff,3 Greg A. Somerville,4,{dagger} Georg Peters,2 Bhanu Sinha,2 Niamh Harraghy,1 Richard A. Proctor,5 and Mathias Herrmann1*

Institute of Medical Microbiology and Hygiene, Institutes of Infectious Disease Medicine, University of Saarland, Homburg/Saar, Germany,1 Institute of Medical Microbiology, University Hospital of Münster, Münster, Germany,2 Institute of Medical Microbiology, University of Zurich, Zurich, Switzerland,3 Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana,4 Department of Medicine and Medical Microbiology and Immunology, University of Wisconsin Medical School, Madison, Wisconsin5

Received 12 November 2004/ Accepted 29 March 2005

The ability of Staphylococcus aureus to adapt to various conditions of stress is the result of a complex regulatory response. Previously, it has been demonstrated that Clp homologues are important for a variety of stress conditions, and our laboratory has shown that a clpC homologue was highly expressed in the S. aureus strain DSM20231during biofilm formation relative to expression in planktonic cells. Persistence and long-term survival are a hallmark of biofilm-associated staphylococcal infections, as cure frequently fails even in the presence of bactericidal antimicrobials. To determine the role of clpC in this context, we performed metabolic, gene expression, and long-term growth and survival analyses of DSM20231as well as an isogenic clpC allelic-replacement mutant, a sigB mutant, and a clpC sigB double mutant. As expected, the clpC mutant showed increased sensitivity to oxidative and heat stresses. Unanticipated, however, was the reduced expression of the tricarboxylic acid (TCA) cycle gene citB (encoding aconitase), resulting in the loss of aconitase activity and preventing the catabolization of acetate during the stationary phase. clpC inactivation abolished post-stationary-phase recovery but also resulted in significantly enhanced stationary-phase survival compared to that of the wild-type strain. These data demonstrate the critical role of the ClpC ATPase in regulating the TCA cycle and implicate ClpC as being important for recovery from the stationary phase and also for entering the death phase. Understanding the stationary- and post-stationary-phase recovery in S. aureus may have important clinical implications, as little is known about the mechanisms of long-term persistence of chronic S. aureus infections associated with formation of biofilms.

* Corresponding author. Mailing address: Kirrberger Str., Building 43, Homburg/Saar 66421, Germany. Phone: 49-6841-162-3900. Fax: 49-6841-162-3985. E-mail:mathias.herrmann{at}uniklinik-saarland.de.

{dagger} Present address: Department of Veterinary and Biomedical Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska.

Journal of Bacteriology, July 2005, p. 4488-4496, Vol. 187, No. 13
0021-9193/05/$08.00+0     doi:10.1128/JB.187.13.4488-4496.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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