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MBE Advance Access published online on February 1, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msj103
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© The Author 2006. 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
Accepted January 30, 2006

Research Article

The Evolutionary Origin of Peroxisomes: An ER-Peroxisome Connection

Agatha Schlüter 1, Raymond Ripp 2, Stéphane Fourcade 3, Jean Louis Mandel 2, Olivier Poch 2, and Aurora Pujol 4 *

1 Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP/Collège de France, 1 rue Laurent Fries, BP10142 67404 Illkirch Cedex, France; Centre de Genètica Mèdica i Molecular. IRO/IDIBELL Hospital Duran i Reynals Granvia Km 2,7. 08907 Hospitalet de Llobregat, Spain
2 Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP/Collège de France, 1 rue Laurent Fries, BP10142 67404 Illkirch Cedex, France
3 Centre de Genètica Mèdica i Molecular. IRO/IDIBELL Hospital Duran i Reynals Granvia Km 2,7. 08907 Hospitalet de Llobregat, Spain
4 Centre de Genètica Mèdica i Molecular. IRO/IDIBELL Hospital Duran i Reynals Granvia Km 2,7. 08907 Hospitalet de Llobregat, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA)

* To whom correspondence should be addressed.
Aurora Pujol, E-mail: apujol{at}igbmc.u-strasbg.fr


  Abstract

The peroxisome is an essential eukaryotic organelle, crucial for lipid metabolism and free radical detoxification, development, differentiation and morphogenesis from yeasts to humans. Loss of peroxisomes invariably leads to fatal peroxisome biogenesis disorders in man (PBD). The evolutionary origin of peroxisomes remains unsolved; proposals for either a symbiogenetic or cellular membrane invagination events are unconclusive. To address this question, we have probed with a peroxisomal proteome, an ensemble of 19 representative eukaryotic complete genomes. Molecular phylogenetic and sequence comparison tools allowed us to identify 4 proteins as peroxisomal markers for unequivocal in silico peroxisome detection. We have then detected the Apicomplexa phylum as a first group of organisms devoid of peroxisomes, in the presence of mitochondria. Finally, we deliver evidence against a prokaryotic ancestor of peroxisomes: a) The peroxisomal membrane is composed of purely eukaryotic bricks and is thus useful to trace the eukaryotes in their evolutionary paths; b) The peroxisomal matrix protein import system shares mechanistic similarities with the endoplasmic reticulum/proteasome degradation process (ERAD), indicating a common evolutionary history.

Keywords: peroxisome; endoplasmic reticulum; functional genomics; peroxisomal markers.
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