Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features

  1. Evelyne Derellea,b,
  2. Conchita Ferrazb,c,
  3. Stephane Rombautsb,d,
  4. Pierre Rouzéb,e,
  5. Alexandra Z. Wordenf,
  6. Steven Robbensd,
  7. Frédéric Partenskyg,
  8. Sven Degroeved,h,
  9. Sophie Echeyniéc,
  10. Richard Cookei,
  11. Yvan Saeysd,
  12. Jan Wuytsd,
  13. Kamel Jabbarij,
  14. Chris Bowlerk,
  15. Olivier Panaudi,
  16. Benoît Piégui,
  17. Steven G. Ballk,
  18. Jean-Philippe Ralk,
  19. François-Yves Bougeta,
  20. Gwenael Piganeaua,
  21. Bernard De Baetsh,
  22. André Picarda,l,
  23. Michel Delsenyi,
  24. Jacques Demaillec,
  25. Yves Van de Peerd,m, and
  26. Hervé Moreaua,m
  1. aObservatoire Océanologique, Laboratoire Arago, Unité Mixte de Recherche 7628, Centre National de la Recherche Scientifique–Université Pierre et Marie Curie-Paris 6, BP44, 66651 Banyuls sur Mer Cedex, France;
  2. cInstitut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 141 Rue de Cardonille, 34396 Montpellier Cedex 5, France;
  3. dDepartment of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology and
  4. eLaboratoire Associé de l’Institut National de la Recherche Agronomique (France), Ghent University, Technologiepark 927, 9052 Ghent, Belgium;
  5. fRosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149;
  6. gStation Biologique, Unité Mixte de Recherche 7144, Centre National de la Recherche Scientifique–Université Pierre et Marie Curie-Paris 6, BP74, 29682 Roscoff Cedex, France;
  7. hDepartment of Applied Mathematics, Biometrics and Process Control, Ghent University, Coupure Links 653, 9000 Ghent, Belgium;
  8. iGénome et Développement des Plantes, Unité Mixte de Recherche 5096, Centre National de la Recherche Scientifique–Université de Perpignan, 52, Avenue de Villeneuve, 66860 Perpignan, France;
  9. jDépartement de Biologie, Formation de Recherche en Evolution 2910, Centre National de la Recherche Scientifique–Ecole Normale Supérieure, 46 Rue d’Ulm, 75230 Paris Cedex 05, France; and
  10. kLaboratoire de Chimie Biologique, Unité Mixte de Recherche 8765, Centre National de la Recherche Scientifique–Université Sciences et Technologies de Lille, 59655 Villeneuve d’Ascq, France

  1. Communicated by Marc C. E. Van Montagu, Ghent University, Ghent, Belgium, June 8, 2006

  2. ↵ bE.D., C.F., S.R., and P.R. contributed equally to this work. (received for review January 4, 2006)

Abstract

The green lineage is reportedly 1,500 million years old, evolving shortly after the endosymbiosis event that gave rise to early photosynthetic eukaryotes. In this study, we unveil the complete genome sequence of an ancient member of this lineage, the unicellular green alga Ostreococcus tauri (Prasinophyceae). This cosmopolitan marine primary producer is the world’s smallest free-living eukaryote known to date. Features likely reflecting optimization of environmentally relevant pathways, including resource acquisition, unusual photosynthesis apparatus, and genes potentially involved in C4 photosynthesis, were observed, as was downsizing of many gene families. Overall, the 12.56-Mb nuclear genome has an extremely high gene density, in part because of extensive reduction of intergenic regions and other forms of compaction such as gene fusion. However, the genome is structurally complex. It exhibits previously unobserved levels of heterogeneity for a eukaryote. Two chromosomes differ structurally from the other eighteen. Both have a significantly biased G+C content, and, remarkably, they contain the majority of transposable elements. Many chromosome 2 genes also have unique codon usage and splicing, but phylogenetic analysis and composition do not support alien gene origin. In contrast, most chromosome 19 genes show no similarity to green lineage genes and a large number of them are specialized in cell surface processes. Taken together, the complete genome sequence, unusual features, and downsized gene families, make O. tauri an ideal model system for research on eukaryotic genome evolution, including chromosome specialization and green lineage ancestry.

Footnotes

  • mTo whom correspondence may be addressed. E-mail: yves.vandepeer{at}psb.ugent.be or h.moreau{at}obs-banyuls.fr

  • ↵ lDeceased November 21, 2004.

  • Author contributions: P.R., B.D.B., Y.V.d.P., and H.M. designed research; S. Rombauts, P.R., A.Z.W., S. Robbens, F.P., S.D., Y.S., J.W., and B.D.B. performed research; C.F., R.C., O.P., B.P., M.D., and J.D. contributed new reagents/analytic tools; E.D., C.F., S. Rombauts, P.R., A.Z.W., S. Robbens, F.P., S.D., S.E., K.J., C.B., S.G.B., J.-P.R., F.-Y.B., G.P., A.P., and J.D. analyzed data; and E.D., A.Z.W., Y.V.d.P., and H.M. wrote the paper.

  • Conflict of interest statement: No conflicts declared.

  • Data deposition: The genome data have been submitted to the European Molecular Biology Laboratory, www.embl.org [accession nos. CR954201 (Chrom 1), CR954202 (Chrom 2), CR954203 (Chrom 3), CR954204 (Chrom 4), CR954205 (Chrom 5), CR954206 (Chrom 6), CR954207 (Chrom 7), CR954208 (Chrom 8), CR954209 (Chrom 9), CR954210 (Chrom10), CR954211 (Chrom 11), CR954212 (Chrom 12), CR954213 (Chrom 13), CR954214 (Chrom 14), CR954215 (Chrom 15), CR954216 (Chrom 16), CR954217 (Chrom 17), CR954218 (Chrom 18), CR954219 (Chrom 19), and CR954220 (Chrom 20)].

  • See Commentary on page 11433.

  • Abbreviation:
    TE,
    transposable element.
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  1. Published online before print July 25, 2006, doi: 10.1073/pnas.0604795103 PNAS August 1, 2006 vol. 103 no. 31 11647-11652
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