Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs
Bruce A. Curtis,
Goro Tanifuji,
Fabien Burki,
Ansgar Gruber,
Manuel Irimia,
Shinichiro Maruyama,
Maria C. Arias,
Steven G. Ball,
Gillian H. Gile,
Yoshihisa Hirakawa,
Julia F. Hopkins,
Alan Kuo,
Stefan A. Rensing,
Jeremy Schmutz,
Aikaterini Symeonidi,
Marek Elias,
Robert J. M. Eveleigh,
Emily K. Herman,
Mary J. Klute,
Takuro Nakayama,
Miroslav Oborník,
Adrian Reyes-Prieto,
E. Virginia Armbrust,
Stephen J. Aves,
Robert G. Beiko,
Pedro Coutinho,
Joel B. Dacks,
Dion G. Durnford,
Naomi M. Fast,
Beverley R. Green,
Cameron J. Grisdale,
Franziska Hempel,
Bernard Henrissat,
Marc P. Höppner,
Ken-Ichiro Ishida,
Eunsoo Kim,
Luděk Kořený,
Peter G. Kroth,
Yuan Liu,
Shehre-Banoo Malik,
Uwe G. Maier,
Darcy McRose,
Thomas Mock,
Jonathan A. D. Neilson,
Naoko T. Onodera,
Anthony M. Poole,
Ellen J. Pritham,
Thomas A. Richards,
Gabrielle Rocap,
Scott W. Roy,
Chihiro Sarai,
Sarah Schaack,
Shu Shirato,
Claudio H. Slamovits,
David F. Spencer,
Shigekatsu Suzuki,
Alexandra Z. Worden,
Stefan Zauner,
Kerrie Barry,
Callum Bell,
Arvind K. Bharti,
John A. Crow,
Jane Grimwood,
Robin Kramer,
Erika Lindquist,
Susan Lucas,
Asaf Salamov,
Geoffrey I. McFadden,
Christopher E. Lane,
Patrick J. Keeling,
Michael W. Gray,
Igor V. Grigoriev and
John M. Archibald ()
Additional contact information
Bruce A. Curtis: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Goro Tanifuji: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Fabien Burki: Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
Ansgar Gruber: Fachbereich Biologie, Universität Konstanz, 78457 Konstanz, Germany
Manuel Irimia: University of Toronto, Toronto, Ontario M5S 3E1, Canada
Shinichiro Maruyama: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Maria C. Arias: Unité de Glycobiologie Structurale et Fonctionnelle, UMR 8576 CNRS-USTL, Université des Sciences et Technologies de Lille, 59655 Villeneuve d’Ascq Cedex, France
Steven G. Ball: Unité de Glycobiologie Structurale et Fonctionnelle, UMR 8576 CNRS-USTL, Université des Sciences et Technologies de Lille, 59655 Villeneuve d’Ascq Cedex, France
Gillian H. Gile: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Yoshihisa Hirakawa: Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
Julia F. Hopkins: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Alan Kuo: US Department of Energy Joint Genome Institute
Stefan A. Rensing: Faculty of Biology and BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79085 Freiburg, Germany
Jeremy Schmutz: US Department of Energy Joint Genome Institute
Aikaterini Symeonidi: Faculty of Biology and BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79085 Freiburg, Germany
Marek Elias: University of Ostrava, Faculty of Science, Life Science Research Centre, 710 00 Ostrava, Czech Republic
Robert J. M. Eveleigh: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Emily K. Herman: University of Alberta, Edmonton, Alberta T6G 2H7, Canada
Mary J. Klute: University of Alberta, Edmonton, Alberta T6G 2H7, Canada
Takuro Nakayama: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Miroslav Oborník: University of South Bohemia, Faculty of Science, Branišovská 31, 37005 České Budějovice, Czech Republic
Adrian Reyes-Prieto: Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
E. Virginia Armbrust: School of Oceanography, University of Washington
Stephen J. Aves: Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
Robert G. Beiko: Faculty of Computer Science, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Pedro Coutinho: Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, CNRS UMR 7257, 163 avenue de Luminy, 13228 Marseille, France
Joel B. Dacks: University of Alberta, Edmonton, Alberta T6G 2H7, Canada
Dion G. Durnford: University of New Brunswick, Fredericton, New Brunswick E3B 5A3, Canada
Naomi M. Fast: University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
Beverley R. Green: University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
Cameron J. Grisdale: University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
Franziska Hempel: LOEWE-Zentrum für Synthetische Mikrobiologie (Synmikro), Hans-Meerwein-Straße, D-35032 Marbug, Germany
Bernard Henrissat: Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, CNRS UMR 7257, 163 avenue de Luminy, 13228 Marseille, France
Marc P. Höppner: Science for Life Laboratory, SE-751 23 Uppsala, Sweden
Ken-Ichiro Ishida: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
Eunsoo Kim: American Museum of Natural History
Luděk Kořený: University of South Bohemia, Faculty of Science, Branišovská 31, 37005 České Budějovice, Czech Republic
Peter G. Kroth: Fachbereich Biologie, Universität Konstanz, 78457 Konstanz, Germany
Yuan Liu: Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
Shehre-Banoo Malik: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Uwe G. Maier: LOEWE-Zentrum für Synthetische Mikrobiologie (Synmikro), Hans-Meerwein-Straße, D-35032 Marbug, Germany
Darcy McRose: Monterey Bay Aquarium Research Institute (MBARI), 7700 Sandholdt Road
Thomas Mock: School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR47TJ, UK
Jonathan A. D. Neilson: University of New Brunswick, Fredericton, New Brunswick E3B 5A3, Canada
Naoko T. Onodera: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Anthony M. Poole: Biomolecular Interaction Centre & School of Biological Sciences, University of Canterbury, Christchurch 8140, New Zealand
Ellen J. Pritham: Eccles Institute of Human Genetics
Thomas A. Richards: The Natural History Museum, Cromwell Road, London SW7 5BD, UK
Gabrielle Rocap: School of Oceanography, University of Washington
Scott W. Roy: San Francisco State University
Chihiro Sarai: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
Sarah Schaack: Reed College
Shu Shirato: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
Claudio H. Slamovits: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
David F. Spencer: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Shigekatsu Suzuki: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
Alexandra Z. Worden: Monterey Bay Aquarium Research Institute (MBARI), 7700 Sandholdt Road
Stefan Zauner: LOEWE-Zentrum für Synthetische Mikrobiologie (Synmikro), Hans-Meerwein-Straße, D-35032 Marbug, Germany
Kerrie Barry: US Department of Energy Joint Genome Institute
Callum Bell: National Center for Genome Resources, Rodeo Park Drive East
Arvind K. Bharti: National Center for Genome Resources, Rodeo Park Drive East
John A. Crow: National Center for Genome Resources, Rodeo Park Drive East
Jane Grimwood: US Department of Energy Joint Genome Institute
Robin Kramer: National Center for Genome Resources, Rodeo Park Drive East
Erika Lindquist: US Department of Energy Joint Genome Institute
Susan Lucas: US Department of Energy Joint Genome Institute
Asaf Salamov: US Department of Energy Joint Genome Institute
Geoffrey I. McFadden: School of Botany, University of Melbourne, Victoria 3010, Australia
Christopher E. Lane: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Patrick J. Keeling: Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
Michael W. Gray: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Igor V. Grigoriev: US Department of Energy Joint Genome Institute
John M. Archibald: Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
Nature, 2012, vol. 492, issue 7427, 59-65
Abstract:
Abstract Cryptophyte and chlorarachniophyte algae are transitional forms in the widespread secondary endosymbiotic acquisition of photosynthesis by engulfment of eukaryotic algae. Unlike most secondary plastid-bearing algae, miniaturized versions of the endosymbiont nuclei (nucleomorphs) persist in cryptophytes and chlorarachniophytes. To determine why, and to address other fundamental questions about eukaryote–eukaryote endosymbiosis, we sequenced the nuclear genomes of the cryptophyte Guillardia theta and the chlorarachniophyte Bigelowiella natans. Both genomes have >21,000 protein genes and are intron rich, and B. natans exhibits unprecedented alternative splicing for a single-celled organism. Phylogenomic analyses and subcellular targeting predictions reveal extensive genetic and biochemical mosaicism, with both host- and endosymbiont-derived genes servicing the mitochondrion, the host cell cytosol, the plastid and the remnant endosymbiont cytosol of both algae. Mitochondrion-to-nucleus gene transfer still occurs in both organisms but plastid-to-nucleus and nucleomorph-to-nucleus transfers do not, which explains why a small residue of essential genes remains locked in each nucleomorph.
Date: 2012
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DOI: 10.1038/nature11681
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