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J. Biol. Chem., Vol. 281, Issue 15, 9909-9918, April 14, 2006

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Pyruvate Formate-lyase and a Novel Route of Eukaryotic ATP Synthesis in Chlamydomonas Mitochondria^*

Ariane Atteia¹, Robert van Lis, Gabriel Gelius-Dietrich, Annie Adrait^¶, Jérôme Garin^¶, Jacques Joyard, Norbert Rolland, and William Martin

From the Institute of Botany, University of Düsseldorf, 40225 Düsseldorf, Germany, the Laboratoire de Physiologie Cellulaire Végétale, UMR5168, CNRS/UJF/INRA/CEA, 38054 Grenoble, France, and the ^¶Laboratoire de Chimie des Protéines, ERM-0201 INSERM/CEA, 38054 Grenoble, France

Pyruvate formate-lyase (PFL) catalyzes the non-oxidative conversion of pyruvate to formate and acetyl-CoA. PFL and its activating enzyme (PFL-AE) are common among strict anaerobic and microaerophilic prokaryotes but are very rare among eukaryotes. In a proteome survey of isolated Chlamydomonas reinhardtii mitochondria, we found several PFL-specific peptides leading to the identification of cDNAs for PFL and PFL-AE, establishing the existence of a PFL system in this photosynthetic algae. Anaerobiosis and darkness led to increased PFL transcripts but had little effect on protein levels, as determined with antiserum raised against C. reinhardtii PFL. Protein blots revealed the occurrence of PFL in both chloroplast and mitochondria purified from aerobically grown cells. Mass spectrometry sequencing of C. reinhardtii mitochondrial proteins, furthermore, identified peptides for phosphotransacetylase and acetate kinase. The phosphotransacetylase-acetate kinase pathway is a common route of ATP synthesis or acetate assimilation among prokaryotes but is novel among eukaryotes. In addition to PFL and pyruvate dehydrogenase, the algae also expresses pyruvate:ferredoxin oxidoreductase and bifunctional aldehyde/alcohol dehydrogenase. Among eukaryotes, the oxygen producer C. reinhardtii has the broadest repertoire of pyruvate-, ethanol-, and acetate-metabolizing enzymes described to date, many of which were previously viewed as specific to anaerobic eukaryotic lineages.

Received for publication, July 19, 2005 , and in revised form, February 1, 2006.

^* This work was supported by grants from the Deutsche Forschungsgemeinschaft (to W. M. and A. Atteia), the CNRS-Département des Sciences de la Vie, and the Fondation Rhône-Alpes (to A. A.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. I–IV.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AJ620190 [GenBank] (ADHE), AJ620191 [GenBank] (PFL), and AJ620192 [GenBank] (PFL-AE).

¹ To whom correspondence should be addressed: Laboratoire de Physiologie Végétale, UMR5168, CNRS/UJF/INRA/CEA Grenoble, 17 rue des Martyrs, 38054 Grenoble, France. Tel.: 33-4-38-78-56-60; Fax: 33-4-38-78-50-91; E-mail: aatteia{at}cea.fr.

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