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J. Biol. Chem., Vol. 279, Issue 37, 38618-38625, September 10, 2004

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Transcriptional Control of the Antimicrobial Peptide Resistance ugtL Gene by the Salmonella PhoP and SlyA Regulatory Proteins^*

Yixin Shi, Tammy Latifi, Michael J. Cromie, and Eduardo A. Groisman¶

From the Department of Molecular Microbiology and the Howard Hughes Medical Institute, Washington University School of Medicine, St. Louis, Missouri, 63110

The PhoP/PhoQ two-component system is a master regulator that governs the ability of Salmonella to cause a lethal infection in mice, the adaptation to low Mg²⁺ environments, and resistance to a variety of antimicrobial peptides. We have recently established that the PhoP-activated ugtL gene is required for resistance to the antimicrobial peptides magainin 2 and polymyxin B. Here we report that ugtL transcription requires not only the PhoP protein but also the virulence regulatory protein SlyA. The PhoP protein footprinted two regions of the ugtL promoter, mutation of either one of which was sufficient to abolish ugtL transcription. Although the SlyA protein is a transcriptional activator of the ugtL gene, it footprinted the ugtL promoter at a region located downstream of the transcription start site. The PhoP protein footprinted the slyA promoter, indicating that it controls slyA transcription directly. The slyA mutant was hypersensitive to magainin 2 and polymyxin B, suggesting that the virulence attenuation exhibited by slyA mutants may be caused by hypersensitivity to antimicrobial peptides. We propose that the PhoP and SlyA proteins control ugtL transcription using a feed-forward loop design.

Received for publication, June 2, 2004 , and in revised form, June 18, 2004.

^* This work was supported by Grant AI49561 from the National Institutes of Health (to E. A. G.). 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.

^¶ Investigator of the Howard Hughes Medical Institute. To whom correspondence should be addressed: Dept. of Molecular Microbiology, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8230, St. Louis, MO 63110. Tel.: 314-362-3692; Fax: 314-747-8228; E-mail: groisman{at}borcim.wustl.edu.

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