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J. Biol. Chem., Vol. 282, Issue 47, 34077-34084, November 23, 2007

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Thermosensing Coordinates a Cis-regulatory Module for Transcriptional Activation of the Intracellular Virulence System in Salmonella enterica Serovar Typhimurium^*

Nancy Duong¹, Suzanne Osborne¹, Víctor H. Bustamante, Ana M. Tomljenovic, José L. Puente, and Brian K. Coombes^¶2

From the Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario L8N 3Z5, Canada, the Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62251, Mexico, and ^¶Public Health Agency of Canada, Laboratory for Foodborne Zoonoses, Guelph, Ontario N1G 3W4, Canada

The expression of bacterial virulence genes is tightly controlled by the convergence of multiple extracellular signals. As a zoonotic pathogen, virulence gene regulation in Salmonella enterica serovar Typhimurium must be responsive to multiple cues from the general environment as well as from multiple niches within animal and human hosts. Previous work has identified combined magnesium and phosphate limitation as an environmental cue that activates genes required for intracellular virulence. One unanswered question is how virulence genes that are expressed within the host are inhibited in non-host environments that satisfy the phosphate and magnesium limitation cues. We report here that thermosensing is the major mechanism controlling incongruous activation of the intracellular virulence phenotype. Bacteria grown at 30 °C or lower were unable to activate the intracellular type III secretion system even under strong inducing signals such as synthetic medium, contact with macrophages, and exposure to the murine gut. Thermoregulation was fully recapitulated in a Salmonella bongori strain engineered to contain the intracellular virulence genes of S. enterica sv. Typhimurium, suggesting that orthologous thermoregulators were available. Accordingly, virulence gene repression at the nonpermissive temperature required Hha and H-NS, two nucleoid-like proteins involved in virulence gene control. The use of combined environmental cues to control transcriptional "logic gates" allows for transcriptional selectivity of virulence genes that would otherwise be superfluous if activated in the non-host environment. Thus, thermosensing by Salmonella provides integrated control of host niche-specific virulence factors.

Received for publication, August 31, 2007 , and in revised form, September 21, 2007.

^* This work was supported in part by Canadian Institutes of Health Research Operating Grant MOP-82704 (to B. K. C.), the Public Health Agency of Canada, and by Dirección General de Asuntos del Personal Académico Grant PAPIIT IN227306-3 (to J. L. P.). 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.

¹ Supported by research training grants from McMaster University.

² Recipient of a New Investigator Award from the CIHR (MSH-83721) and a Young Investigator Award from the American Society of Microbiology. To whom correspondence should be addressed: Dept. of Biochemistry and Biomedical Sciences, McMaster University, 1200 Main St. West, Health Sciences Centre 4H17, Hamilton, Ontario L8N 3Z5, Canada. Tel.: 905-525-9140 (ext. 22159); Fax: 905-522-9033; E-mail: coombes{at}mcmaster.ca.

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