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Science 10 April 2009:
Vol. 324. no. 5924, pp. 268 - 272
DOI: 10.1126/science.1167222
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Reports

Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas

Alexandra Z. Worden,1* Jae-Hyeok Lee,2{dagger} Thomas Mock,3{dagger}{ddagger} Pierre Rouzé,4{dagger} Melinda P. Simmons,1{dagger} Andrea L. Aerts,5 Andrew E. Allen,6 Marie L. Cuvelier,1,7 Evelyne Derelle,8 Meredith V. Everett,7 Elodie Foulon,9 Jane Grimwood,5,10 Heidrun Gundlach,11 Bernard Henrissat,12 Carolyn Napoli,13 Sarah M. McDonald,1 Micaela S. Parker,3 Stephane Rombauts,4 Aasf Salamov,5 Peter Von Dassow,9 Jonathan H. Badger,6 Pedro M. Coutinho,11 Elif Demir,1 Inna Dubchak,5 Chelle Gentemann,14 Wenche Eikrem,15 Jill E. Gready,16 Uwe John,17 William Lanier,18 Erika A. Lindquist,5 Susan Lucas,5 Klaus F. X. Mayer,10 Herve Moreau,8 Fabrice Not,9 Robert Otillar,5 Olivier Panaud,19 Jasmyn Pangilinan,5 Ian Paulsen,20 Benoit Piegu,19 Aaron Poliakov,5 Steven Robbens,4 Jeremy Schmutz,5,10 Eve Toulza,21 Tania Wyss,22 Alexander Zelensky,23 Kemin Zhou,5 E. Virginia Armbrust,3 Debashish Bhattacharya,18 Ursula W. Goodenough,2 Yves Van de Peer,4 Igor V. Grigoriev5

Picoeukaryotes are a taxonomically diverse group of organisms less than 2 micrometers in diameter. Photosynthetic marine picoeukaryotes in the genus Micromonas thrive in ecosystems ranging from tropical to polar and could serve as sentinel organisms for biogeochemical fluxes of modern oceans during climate change. These broadly distributed primary producers belong to an anciently diverged sister clade to land plants. Although Micromonas isolates have high 18S ribosomal RNA gene identity, we found that genomes from two isolates shared only 90% of their predicted genes. Their independent evolutionary paths were emphasized by distinct riboswitch arrangements as well as the discovery of intronic repeat elements in one isolate, and in metagenomic data, but not in other genomes. Divergence appears to have been facilitated by selection and acquisition processes that actively shape the repertoire of genes that are mutually exclusive between the two isolates differently than the core genes. Analyses of the Micromonas genomes offer valuable insights into ecological differentiation and the dynamic nature of early plant evolution.

1 Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039 USA.
2 Department of Biology, Washington University at St. Louis, St. Louis, MO 63130, USA.
3 School of Oceanography, University of Washington, Seattle, WA 98195, USA.
4 Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB) and Department of Molecular Genetics, Ghent University, 9052 Gent, Belgium.
5 U.S. Department of Energy (DOE) Joint Genome Institute (JGI), Walnut Creek, CA 94598, USA.
6 J. Craig Venter Institute, San Diego, CA 92121, USA.
7 Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL 33149, USA.
8 Observatoire Océanologique, CNRS–Université Pierre et Marie Curie, 66651 Banyuls sur Mer, France.
9 Station Biologique de Roscoff, CNRS–Université Pierre et Marie Curie, Roscoff Cedex, France.
10 Stanford Human Genome Center, Stanford University School of Medicine, Palo Alto, CA 94304, USA.
11 Institute of Bioinformatics and System Biology, German Research Center for Environmental Health, 85764 Neuherberg, Germany.
12 Architecture et Fonction des Macromolécules Biologiques, Universities of Aix-Marseille I and II, Marseille 13288, France.
13 Biology Institute, University of Arizona, Tucson, AZ 85719, USA.
14 Remote Sensing Systems, Santa Rosa, CA 95401, USA.
15 Avdeling for Marinbiologi og Limnologi, University of Oslo, Oslo N-0316, Norway.
16 Division of Molecular Bioscience, College of Medicine, Biology and the Environment, Australian National University, Canberra ACT 2601, Australia.
17 Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen, Bremerhaven 27570, Germany.
18 Department of Biology, University of Iowa, Iowa City, IA 52242, USA.
19 Laboratoire Genome et Development des Plantes Université de Perpignan, 66860 Perpignan, France.
20 Department of Chemistry and Biomolecular Sciences, Macquarie University, New South Wales 2109, Australia.
21 Ecosystèmes Lagunaires, Université Montpellier II, F-34095 Montpellier Cedex 05, France.
22 Department of Biology, University of Miami, Miami, FL 33149, USA.
23 Department of Genetics, Erasmus Medical Center, Rotterdam 3015 CE, Netherlands.

{dagger} These authors contributed equally to this work.

{ddagger} Present address: School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK.

* To whom correspondence should be addressed. E-mail: azworden{at}mbari.org

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