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J. Biol. Chem., Vol. 279, Issue 25, 26453-26461, June 18, 2004

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Supramolecular Organization of Cytochrome c Oxidase- and Alternative Oxidase-dependent Respiratory Chains in the Filamentous Fungus Podospora anserina^*

Frank Krause, Christian Q. Scheckhuber¶, Alexandra Werner¶, Sascha Rexroth, Nicole H. Reifschneider, Norbert A. Dencher, and Heinz D. Osiewacz¶

From the Department of Chemistry, Physical Biochemistry, Darmstadt University of Technology, Petersenstrae 22, D-64287 Darmstadt, Germany and ^¶Botanical Institute, Johann Wolfgang Goethe-University, Marie-Curie-Strasse 9, D-60439 Frankfurt am Main, Germany

To elucidate the molecular basis of the link between respiration and longevity, we have studied the organization of the respiratory chain of a wild-type strain and of two long-lived mutants of the filamentous fungus Podospora anserina. This established aging model is able to respire by either the standard or the alternative pathway. In the latter pathway, electrons are directly transferred from ubiquinol to the alternative oxidase and thus bypass complexes III and IV. We show that the cytochrome c oxidase pathway is organized according to the mammalian "respirasome" model (Schägger, H., and Pfeiffer, K. (2000) EMBO J. 19, 1777–1783). In contrast, the alternative pathway is composed of distinct supercomplexes of complexes I and III (i.e. I₂ and I₂III₂), which have not been described so far. Enzymatic analysis reveals distinct functional properties of complexes I and III belonging to either cytochrome c oxidase- or alternative oxidase-dependent pathways. By a gentle colorless-native PAGE, almost all of the ATP synthases from mitochondria respiring by either pathway were preserved in the dimeric state. Our data are of significance for the understanding of both respiratory pathways as well as lifespan control and aging.

Received for publication, September 24, 2003

^* This work was supported in part by the Deutsche Forschungsge-meinschaft Grant SFB 472 (to N. A. D. and Dr. Holger Seelert) and Grant Os75/5-3 (to H. D. O.), by Fonds der Chemischen Industrie, and by Grant 03-DE5DA1-8 from the Bundesministerium für Bildung und Forschung (to N. A. D.). 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.: 49-6151-165376; Fax: 49-6151-164171; E-mail: f_krause{at}pop.tu-darmstadt.de.

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