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MBE Advance Access published online on July 27, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msi220
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© The Author 2005. 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@oupjournals.org
Accepted July 7, 2005

Research Article

New Insights into the Nature and Phylogeny of Prasinophyte Antenna Proteins: Ostreococcus tauri, a Case Study

Christophe Six 1 *, Alexandra Z. Worden 2 *, Francisco Rodríguez 1, Hervé Moreau 3, and Frédéric Partensky 1*

1 Station Biologique, UMR 7144 CNRS-UPMC, BP74, 29682 Roscoff cedex, France
2 Rosenstiel School of Marine & Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway Miami, FL 33149-1098 USA
3 Laboratoire Arago, UMR 7628 CNRS-UPMC, BP44, 66651 Banyuls sur mer cedex, France

* To whom correspondence should be addressed.
Frédéric Partensky, E-mail: partensky{at}sb-roscoff.fr


  Abstract

The basal position of the Mamiellales (Prasinophyceae) within the green lineage makes these unicellular organisms key to elucidating early stages in the evolution of chlorophyll a/b-binding light-harvesting complexes (LHCs). Here, we unveil the complete and unexpected diversity of Lhc proteins in Ostreococcus tauri, a member of the Mamiellales order, based on results from complete genome sequencing. Like Mantoniella squamata, O. tauri possesses a number of genes encoding an unusual prasinophyte-specific Lhc protein type herein designated "Lhcp". Biochemical characterization of the complexes revealed that these polypeptides, which bind chlorophylls a, b, and a chlorophyll c-like pigment (Mg-2,4-divinyl phaeoporphyrin a5 monomethyl ester) as well as a number of unusual carotenoids, are likely predominant. They are retrieved to some extent in both reaction center I- (RCI-) and RCII-enriched fractions, suggesting a possible association to both PSs. However, in sharp contrast to previous reports on LHCs of M. squamata, O. tauri also possesses other LHC subpopulations, including LHCI proteins (encoded by 5 distinct Lhca genes) and the minor LHCII polypeptides CP26 and CP29. Using an antibody against plant Lhca2, we unambiguously show that LHCI proteins are present not only in O. tauri, in which they are likely associated to RCI, but also other Mamiellales, including M. squamata. With the exception of Lhcp genes, all the identified Lhc genes are present in single copy only. Overall, the discovery of LHCI proteins in these prasinophytes, combined with the lack of the major LHCII polypeptides found in higher plants or other green algae, supports the hypothesis that the latter proteins appeared subsequent to LHCI proteins. The major LHC of prasinophytes might have arisen prior to the LHCII of other chlorophyll a/b-containing organisms, possibly by divergence of a LHCI gene precursor. However, the discovery in O. tauri of CP26-like proteins, phylogenetically placed at the base of the major LHCII protein clades, yields new insight to the origin of these antenna proteins, which have evolved separately in higher plants and green algae. Its diverse but numerically limited suite of Lhc genes renders O. tauri an exceptional model system for future research on the evolution and function of LHC components.

Keywords: Ostreococcus tauri; Prasinophyceae; Light-harvesting complex; evolution; phylogeny.

*These authors contributed equally to this work.


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