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MBE Advance Access published online on April 6, 2009

Molecular Biology and Evolution, doi:10.1093/molbev/msp068
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the {alpha}-proteobacterial mitochondrial ancestor

Ariane Atteia1,2,*, Annie Adrait3, Sabine Brugière3, Marianne Tardif3, Robert van Lis1,2, Oliver Deusch4, Tal Dagan4, Lauriane Kuhn3, Brigitte Gontero2, William Martin4, Jérôme Garin3, Jacques Joyard1 and Norbert Rolland1

1 Laboratoire de Physiologie Cellulaire Végétale, CNRS, UMR5168, F-38054 Grenoble, France; CEA, DSV, iRTSV, F-38054 Grenoble, France; INRA, UMR1200, F-38054 Grenoble, France; Université Joseph Fourier, F-38054, Grenoble, France
2 Unité de Bioénergétique et Ingénierie des Protéines, CNRS, UPR9036-IFR 88, 31 Chemin Joseph Aiguier, F-13402 Marseille, France
3 CEA, DSV, iRTSV, Laboratoire d'Etude de la Dynamique des Protéomes, Grenoble, F-38054, France; INSERM, U880, Grenoble, F-38054, France; Université Joseph Fourier, Grenoble, F-38054, France
4 Institute of Botany, University of Düsseldorf, Germany

* Author for correspondence. Ariane.Atteia{at}ifr88.cnrs-mrs.fr

Address for correspondence Unité de Bioénergétique et Ingénierie des Protéines, CNRS, UPR9036-IFR 88, 31 Chemin Joseph Aiguier, F-13402 Marseille Cedex 20, France. Phone: 33 04 91 16 45 48. FAX: 33 04 91 16 45 78.

Received for publication January 16, 2009. Revision received March 22, 2009. Accepted for publication March 24, 2009.

Mitochondria play a key role in the life and death of eukaryotic cells, yet the full spectrum of mitochondrial functions is far from being fully understood, especially in photosynthetic organisms. To advance our understanding of mitochondrial functions in a photosynthetic cell, an extensive proteomic survey of Percoll-purified mitochondria from the metabolically versatile, hydrogen-producing green alga Chlamydomonas reinhardtii was performed. Different fractions of purified mitochondria from Chlamydomonas cells grown under aerobic conditions were analyzed by nano-liquid chromatography-electrospray ionization-mass spectrometry (MS) after protein separation on SDS-PAGE or on blue-native (BN)-PAGE. Of the 496 non-redundant proteins identified, 149 are known or predicted to reside in other cellular compartments and were thus excluded from the molecular and evolutionary analyses of the Chlamydomonas proteome. The mitochondrial proteome of the photosynthetic alga reveals important lineage-specific differences with other mitochondrial proteomes, reflecting the high metabolic diversity of the organelle. Some mitochondrial metabolic pathways in Chlamydomonas appear to combine typical mitochondrial enzymes and bacterial-type ones whereas others are unknown among mitochondriate eukaryotes. The comparison of the Chlamydomonas proteins to their identifiable homologs predicted from 354 sequenced genomes indicated that Arabidopsis is the most closely related non-algal eukaryote. Furthermore, this phylogenomic analysis shows that free-living {alpha}-proteobacteria from the metabolically versatile orders Rhizobiales and Rhodobacterales better reflect the gene content of the ancestor of the chlorophyte mitochondria than parasitic {alpha}-proteobacteria with reduced and specialized genomes.

Key Words: Chlamydomonas • endosymbiont • metabolism • phylogeny • proteome


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