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Journal of Bacteriology, July 2009, p. 4419-4426, Vol. 191, No. 13
0021-9193/09/$08.00+0     doi:10.1128/JB.00321-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

ResDE-Dependent Regulation of Enterotoxin Gene Expression in Bacillus cereus: Evidence for Multiple Modes of Binding for ResD and Interaction with Fnr{triangledown} ,{dagger}

Julia Esbelin,1,2 Jean Armengaud,3 Assia Zigha,1,2,# and Catherine Duport1,2*

Université d'Avignon et des Pays de Vaucluse, UMR408, Sécurité et Qualité des Produits d'Origine Végétale; INRA, Avignon F-84000, France,1 INRA, UMR408, Sécurité et Qualité des Produits d'Origine Végétale; INRA, Avignon F-84000, France,2 CEA, DSV, IBEB, Lab Biochim System Perturb, Bagnols-sur-Cèze F-30207, France3

Received 9 March 2009/ Accepted 17 April 2009

In the food-borne pathogen Bacillus cereus F4430/73, the production of major virulence factors hemolysin BL (Hbl) and nonhemolytic enterotoxin (Nhe) is regulated through complex mechanisms. The two-component regulatory system ResDE is involved in the activation of hbl and nhe transcription. Here, the response regulator ResD and the sensor kinase ResE were overexpressed and purified, and autophosphorylation of ResE and transphosphorylation of ResD by ResE were demonstrated in vitro. ResD is mainly monomeric in solution, regardless of its phosphorylation state. ResD was shown to interact directly with promoter regions (p) of the enterotoxin regulator genes resDE, fnr, and plcR and the enterotoxin structural genes nhe and hbl, but with different affinities. Binding of ResD to pplcR, pnhe, and phbl was not dependent on the ResD phosphorylation status. In contrast, ResD phosphorylation significantly increased interactions between ResD and presDE and pfnr. Taken together, these results showed that phosphorylation of ResD results in a different target expression pattern. Furthermore, ResD and the redox activator Fnr were found to physically interact and simultaneously bind their target DNAs. We propose that unphosphorylated ResD acts as an antiactivator of Fnr, while phosphorylated ResD acts as a coactivator of Fnr. Finally, our findings represent the first molecular evidence of the role of ResDE as a sentinel system capable of sensing redox changes and coordinating a response that modulates B. cereus virulence.

* Corresponding author. Mailing address: UMR408, INRA, Site Agroparc, 84914 Avignon cedex 9, France. Phone: 33 4 32 72 25 07. Fax: 33 4 32 72 24 92. E-mail: catherine.duport{at}univ-avignon.fr

{triangledown} Published ahead of print on 24 April 2009.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

# Present address: Metabolic Explorer, Biopôle Clermont-Limagne, 63360 Saint-Beauzire F-63360, France.

Journal of Bacteriology, July 2009, p. 4419-4426, Vol. 191, No. 13
0021-9193/09/$08.00+0     doi:10.1128/JB.00321-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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