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J. Biol. Chem., Vol. 280, Issue 29, 26760-26769, July 22, 2005

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Analysis of the Heteromeric CsdA-CsdE Cysteine Desulfurase, Assisting Fe-S Cluster Biogenesis in Escherichia coli^*

Laurent Loiseau, Sandrine Ollagnier-de Choudens, David Lascoux¶, Eric Forest¶, Marc Fontecave, and Frédéric Barras||

From the Laboratoire de Chimie Bactérienne, UPR-CNRS 9043, Institut de Biologie Structurale et Microbiologie, 31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France, Laboratoire de Chimie et Biochimie des Centres Rédox Biologiques, DRDC-CB, Commissariat à l'Energie Atomique (Saclay, France)/CNRS/Université Joseph Fourier, UMR 5047, 17 Avenue des Martyrs, 38054 Grenoble Cedex 09, France, and ^¶Laboratoire de Spectrométrie de Masse des Protéines, Institut de Biologie Structurale, Commissariat à l'Energie Atomique (Saclay, France)/CNRS/Université Joseph Fourier, 41 rue J. Horowitz, 38027 Grenoble, Cedex 1, France

Biogenesis of iron-sulfur (Fe-S) cluster-containing proteins relies on assistance of complex machineries. To date three systems, NIF, ISC, and SUF, were reported to allow maturation of Fe-S proteins. Here we report that the csdA-csdE (formally ygdK) genes of Escherichia coli constitute a sulfur-generating system referred to as CSD which also contributes to Fe-S biogenesis in vivo. This conclusion was reached by applying a thorough combination of both in vivo and in vitro strategies and techniques. Yeast two-hybrid analysis allowed us to show that CsdA and CsdE interact. Enzymology analysis showed that CsdA cysteine desulfurase activity is increased 2-fold in the presence of CsdE. Mass spectrometry analysis and site-directed mutagenesis showed that residue Cys-61 from CsdE acted as an acceptor site for sulfur provided by cysteine desulfurase activity of CsdA. Genetic investigations revealed that the csdA-csdE genes could act as multicopy suppressors of iscS mutation. Moreover, both in vitro and in vivo investigations pointed to a specific connection between the CSD system and quinolinate synthetase NadA.

Received for publication, April 14, 2005 , and in revised form, May 3, 2005.

^* This work was supported by grants from the CNRS, the Commissariat à l'Energie Atomique (Saclay, France), the Université Aix-Marseille II and the Université Joseph Fourier, and the ACI Biologie Structurale, Moléculaire et Cellulaire." 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.

^|| To whom correspondence should be addressed. Tel.: 33-4-91-16-45-79; Fax: 33-4-91-71-89-14; E-mail: barras{at}ibsm.cnrs-mrs.fr.

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