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J. Biol. Chem., Vol. 281, Issue 30, 21147-21161, July 28, 2006

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Induction and Function of the Phage Shock Protein Extracytoplasmic Stress Response in Escherichia coli^*

Goran Jovanovic¹, Louise J. Lloyd¹, Michael P. H. Stumpf, Antony J. Mayhew, and Martin Buck²

From the Division of Biology, Sir Alexander Fleming Building, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom and the Centre for Bioinformatics, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom

The phage shock protein (Psp) F regulon response in Escherichia coli is thought to be induced by impaired inner membrane integrity and an associated decrease in proton motive force (pmf). Mechanisms by which the Psp system detects the stress signal and responds have so far remained undetermined. Here we demonstrate that PspA and PspG directly confront a variety of inducing stimuli by switching the cell to anaerobic respiration and fermentation and by down-regulating motility, thereby subtly adjusting and maintaining energy usage and pmf. Additionally, PspG controls iron usage. We show that the Psp-inducing protein IV secretin stress, in the absence of Psp proteins, decreases the pmf in an ArcB-dependent manner and that ArcB is required for amplifying and transducing the stress signal to the PspF regulon. The requirement of the ArcB signal transduction protein for induction of psp provides clear evidence for a direct link between the physiological redox state of the cell, the electron transport chain, and induction of the Psp response. Under normal growth conditions PspA and PspD control the level of activity of ArcB/ArcA system that senses the redox/metabolic state of the cell, whereas under stress conditions PspA, PspD, and PspG deliver their effector functions at least in part by activating ArcB/ArcA through positive feedback.

Received for publication, March 13, 2006 , and in revised form, May 3, 2006.

^* This work was supported by the Wellcome Trust Grant (to M. B.) and by a Wellcome Trust postgraduate studentship (to L. J. L.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. 1 and Tables 1-5.

¹ These authors contributed equally to this work.

² To whom correspondence should be addressed: Tel.: 44-207-594-5442; Fax: 44-207-594-5419; E-mail: m.buck{at}imperial.ac.uk.

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