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J. Biol. Chem., Vol. 280, Issue 11, 10683-10694, March 18, 2005

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BzdR, a Repressor That Controls the Anaerobic Catabolism of Benzoate in Azoarcus sp. CIB, Is the First Member of a New Subfamily of Transcriptional Regulators^*

María J. L. Barragán, Blas Blázquez, María T. Zamarro, José M. Mancheño¶||, José L. García, Eduardo Díaz, and Manuel Carmona||**

From the Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas-CSIC, Ramiro de Maeztu 9, Madrid 28040, Spain and ^¶Grupo de Cristalografía Macromolecular, Instituto de Química-Física Rocasolano-CSIC, Madrid 28006, Spain

In this work, we have studied the transcriptional regulation of the bzd operon involved in the anaerobic catabolism of benzoate in the denitrifying Azoarcus sp. strain CIB. The transcription start site of the P_N promoter running the expression of the bzd catabolic genes was identified. Gel retardation assays and P_N::lacZ translational fusion experiments performed both in Azoarcus sp. CIB and Escherichia coli cells have shown that bzdR encodes a specific repressor that controls the inducible expression of the adjacent bzd catabolic operon, being the first intermediate of the catabolic pathway (i.e. benzoyl-CoA, the actual inducer molecule). This is the first report of a transcriptional repressor and a CoA-derived aromatic inducer controlling gene expression in the anaerobic catabolism of aromatic compounds. DNase I footprinting experiments revealed that BzdR protected three regions (operators) at the P_N promoter. The three operators contain direct repetitions of a TGCA sequence that forms part of longer palindromic structures. In agreement with the repressor role of BzdR, operator region I spans the transcription initiation site as well as the -10 sequence for recognition of the RNA polymerase. Primary sequence analyses of BzdR showed an unusual modular organization with an N-terminal region homologous to members of the HTH-XRE family of transcriptional regulators and a C-terminal region similar to shikimate kinases. A three-dimensional model of the N-terminal and C-terminal regions of BzdR, generated by comparison with the crystal structures of the SinR regulator from Bacillus subtilis and the shikimate kinase I protein from E. coli, strongly suggests that they contain the helix-turn-helix DNA-binding motif and the benzoyl-CoA binding groove, respectively. The BzdR protein constitutes, therefore, the prototype of a new subfamily of transcriptional regulators.

Received for publication, October 29, 2004 , and in revised form, December 13, 2004.

^* This work was supported by Comunidad Autónoma de Madrid Grant 07M/0076/2002 and Comisión Interministerial de Ciencia y Tecnología Grants BIO2003-01482 and VEM2003-20075-CO2-02. 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.

Recipient of a predoctoral fellowship from the Plan Nacional de Formación de Personal Investigador-MEC.

^|| Holder of the Ramón y Cajal Program of the Spanish Ministerio de Educación y Ciencia.

^** To whom correspondence should be addressed: Dept. de Microbiología Molecular, Centro de Investigaciones Biológicas-CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain. Tel.: 34-91-8373112; E-mail: mcarmona{at}cib.csic.es.

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