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Originally published In Press as doi:10.1074/jbc.M709405200 on March 13, 2008

J. Biol. Chem., Vol. 283, Issue 20, 14084-14091, May 16, 2008
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NfuA, a New Factor Required for Maturing Fe/S Proteins in Escherichia coli under Oxidative Stress and Iron Starvation Conditions*Formula

Sandra Angelini§1, Catherine Gerez||**, Sandrine Ollagnier-de Choudens||**, Yiannis Sanakis{ddagger}{ddagger}, Marc Fontecave||**, Frédéric Barras{ddagger}§, and Béatrice Py{ddagger}§2

From the {ddagger}Aix-Marseille II, Campus de Luminy, UniversitédelaMéditerranée, 70 rte Léon Lachamp 13009 Marseille, France, the §Laboratoire de Chimie Bactérienne, CNRS, UPR 9043, 31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France, the Laboratoire de Chimie et Biologie des Métaux, CNRS UMR 5249, 17 Avenue des Martyrs, F-38054 Grenoble, France, the ||Laboratoire de Chimie et Biologie des Métaux, CEA 17 Avenue des Martyrs, F-38054 Grenoble, France, the **Université Joseph Fourier, F-38054 Grenoble, France, and the {ddagger}{ddagger}Institute of Materials Science, NCSR, Demokritos, 15310 Ag, Paraskevi, Attiki, Greece

Iron/sulfur (Fe/S) proteins are central to the functioning of cells in both prokaryotes and eukaryotes. Here, we show that the yhgI gene, which we renamed nfuA, encodes a two-domain protein that is required for Fe/S biogenesis in Escherichia coli. The N-terminal domain resembles the so-called Fe/S A-type scaffold but, curiously, has lost the functionally important Cys residues. The C-terminal domain shares sequence identity with Nfu proteins. Mössbauer and UV-visible spectroscopic analyses revealed that, upon reconstitution, NfuA binds a [4Fe-4S] cluster. Moreover, NfuA can transfer this cluster to apo-aconitase. Mutagenesis studies indicated that the N- and C-terminal domains are important for NfuA function in vivo. Similarly, the functional importance of Cys residues present in the Nfu-like domain was demonstrated in vivo by introducing Cys->Ser mutations. In vivo investigations revealed that the nfuA gene is important for E. coli to sustain oxidative stress and iron starvation. Also, combining nfuA with either isc or suf mutations led to additive phenotypic deficiencies, indicating that NfuA is a bona fide new player in Isc- and Suf-dependent Fe/S biogenesis pathways. Taken together, these data demonstrate that NfuA intervenes in the maturation of apoproteins in E. coli, allowing them to acquire Fe/S clusters. By taking into account results from numerous previous transcriptomic studies that had suggested a link between NfuA and protein misfolding, we discuss the possibility that NfuA could act as a scaffold/chaperone for damaged Fe/S proteins.


Received for publication, November 15, 2007 , and in revised form, January 30, 2008.

* This work was supported in part by grants from the Centre National de la Recherche Scientifique, the Agence Nationale pour la Recherche (Programmes blancs BIOSUF and Stress oxydant), the Centre à l'Energie Atomique, the Université de la Méditerranée (Marseille), the Université Joseph Fourier (Grenoble), and the ACI BCMS from the Ministère de la Recherche. 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.

Formula The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1-S5 and Tables S1 and S2.

1 Supported by a CNRS postdoctoral fellowship.

2 To whom correspondence should be addressed: CNRS, Laboratoire de Chimie Bactérienne, UPR 9043, 31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France. Tel.: 33-0-4-91-16-46-39; Fax: 33-0-4-91-71-89-14; E-mail: py{at}ibsm.cnrs-mrs.fr.


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