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J. Biol. Chem., Vol. 279, Issue 38, 39340-39347, September 17, 2004

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Bacillus subtilis DesR Functions as a Phosphorylation-activated Switch to Control Membrane Lipid Fluidity^*

Larisa E. Cybulski, Gloria del Solar, Patricio O. Craig¶, Manuel Espinosa, and Diego de Mendoza||

From the Instituto de Biología Molecular y Celular de Rosario (IBR), Consejo Nacional de Investigaciones Científicas y Técnicas, and Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, 2002LRK-Rosario, Argentina, the Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, 28040 Madrid, Spain, and the ^¶Instituto Leloir, C1405BWE, Buenos Aires, Argentina

The Des pathway of Bacillus subtilis regulates the synthesis of the cold-shock induced membrane-bound enzyme 5-fatty acid desaturase (5-Des). A central component of the Des pathway is the response regulator, DesR, which is activated by a membrane-associated kinase, DesK, in response to a decrease in membrane lipid fluidity. Despite genetic and biochemical studies, specific details of the interaction between DesR and the DNA remain unknown. In this study we show that only the phosphorylated form of protein DesR is able to bind to a regulatory region immediately upstream of the promoter of the 5-Des gene (Pdes). Phosphorylation of the regulatory domain of dimeric DesR promotes, in a cooperative fashion, the hierarchical occupation of two adjacent, non-identical, DesR-P DNA binding sites, so that there is a shift in the equilibrium toward the tetrameric active form of the response regulator. Subsequently, this phosphorylation signal propagation leads to the activation of the des gene through recruitment of RNA polymerase to Pdes. This is the first dissected example of a transcription factor functioning as a phosphorylation-activated switch for a cold-shock gene, allowing the cell to optimize the fluidity of membrane phospholipids.

Received for publication, May 10, 2004 , and in revised form, July 6, 2004.

^* This work was supported in part by a grant from the Agencia Nacional de Promoción Científica y Tecnológica (FONCyT) (to D. de M.) and Special Action BMC2002-11562-E and SAF2001-05040-E from the Ministerio de Educación Ciencia (to M. E.). 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 Figs. S1–S5 and Tables I and II.

^|| Career investigator from Consejo Nacional de Investigaciones Científicas y Técnicas and an International Research Scholar from the Howard Hughes Medical Institute. To whom correspondence should be addressed: Instituto de Biología Molecular y Celular de Rosario (IBR) and Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Suipacha 531, 2002LRK-Rosario, Argentina. Tel.: 54-341-4351235; Fax: 54-341-4390465; E-mail: diegonet{at}citynet.net.ar.

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