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J. Biol. Chem., Vol. 280, Issue 13, 13004-13011, April 1, 2005

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Evolution of Mitochondrial Oxa Proteins from Bacterial YidC

INHERITED AND ACQUIRED FUNCTIONS OF A CONSERVED PROTEIN INSERTION MACHINERY^*

Marc Preuss, Martin Ott, Soledad Funes, Joen Luirink, and Johannes M. Herrmann¶

From the Institut für Physiologische Chemie, Universität München, Butenandtstrasse 5, 81377 München, Germany and Department of Molecular Microbiology, Institute of Molecular Cell Biology, Vrije Universiteit, De Boelelaan 1087, 1081 HV Amsterdam, The Netherlands

Members of the Oxa1/YidC family are involved in the biogenesis of membrane proteins. In bacteria, YidC catalyzes the insertion and assembly of proteins of the inner membrane. Mitochondria of animals, fungi, and plants harbor two distant homologues of YidC, Oxa1 and Cox18/Oxa2. Oxa1 plays a pivotal role in the integration of mitochondrial translation products into the inner membrane of mitochondria. It contains a C-terminal ribosome-binding domain that physically interacts with mitochondrial ribosomes to facilitate the co-translational insertion of nascent membrane proteins. The molecular function of Cox18/Oxa2 is not well understood. Employing a functional complementation approach with mitochondria-targeted versions of YidC we show that YidC is able to functionally replace both Oxa1 and Cox18/Oxa2. However, to integrate mitochondrial translation products into the inner membrane of mitochondria, the ribosome-binding domain of Oxa1 has to be appended onto YidC. On the contrary, the fusion of the ribosome-binding domain onto YidC prevents its ability to complement COX18 mutants suggesting an indispensable post-translational activity of Cox18/Oxa2. Our observations suggest that during evolution of mitochondria from their bacterial ancestors the two descendents of YidC functionally segregated to perform two distinct activities, one co-translational and one post-translational.

Received for publication, December 15, 2004 , and in revised form, January 14, 2005.

^* This work was supported by Deutsche Forschungsgemeinschaft Grant SFB594, Teilprojekt B05 (to J. M. H.) and by a European Molecular Biology Organization long term fellowship (to S. F.). 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.: 49-89-2180-77122; Fax: 49-89-2180-77093; E-mail: hannes.herrmann{at}bio.med.uni-muenchen.de.

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