Pan genome of the phytoplankton Emiliania underpins its global distribution

Journal name:
Nature
Volume:
499,
Pages:
209–213
Date published:
DOI:
doi:10.1038/nature12221
Received
Accepted
Published online
Corrected online

Coccolithophores have influenced the global climate for over 200 million years1. These marine phytoplankton can account for 20per cent of total carbon fixation in some systems2. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space3. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO2 production or uptake, sequestration and export to the deep ocean4. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions.

At a glance

Figures

  1. Emiliania huxleyi and its position in the eukaryotic tree of life.
    Figure 1: Emiliania huxleyi and its position in the eukaryotic tree of life.

    a, E. huxleyi has five well-characterized calcification morphotypes and an overcalcified state1. b, Cladogram showing the distinct branch occupied by the haptophyte lineage on the basis of RAxML analysis of concatenated, nuclear-encoded proteins after addition of homologues from CCMP1516 and a pico-prymnesiophyte-targeted metagenome8. Lineages with algal taxa are indicated (symbol). Filled circles represent nodes with≥70% bootstrap support. The tree is rooted for display purposes only.

  2. Relative composition of the E. huxleyi genome.
    Figure 2: Relative composition of the E. huxleyi genome.

    Structural composition of genomes from CCMP1516 and the diatom P. tricornutum. Grey-shaded regions of each class depict proportions of tandem repeats and low-complexity regions. The grey vertical box contains only tandem repeats and low-complexity sequence. Pie charts indicate the proportion of non-repeated (white) and repeated or low-complexity (black) sequences in each haploid genome.

  3. Predicted proteome comparisons and concatenated phylogeny of E. huxleyi strains.
    Figure 3: Predicted proteome comparisons and concatenated phylogeny of E. huxleyi strains.

    a, Isolation locations shown over the averaged Reynolds monthly sea-surface temperature (SST) climatology (1985–2007). b, tBLASTn homology search results using predicted CCMP1516 proteins against assemblies from other strains. Bars are coloured according to the number of gene products and nucleotide per cent identity. c, Best Bayesian topology, where node values indicate posterior probability/maximum-likelihood bootstrap support. Haploid genome sizes (in Mb) are provided in brackets (with ND indicating not determined), and shaded boxes denote robust clades of geographically dispersed strains. The variable distribution of nitrite reductase (NirS) and plastocyanin (PetE) is shown.

  4. Distribution of genes in the variable genome reflecting niche specificity.
    Figure 4: Distribution of genes in the variable genome reflecting niche specificity.

    a, Key genes (gene numbers on axes) involved in nutrient acquisition and metabolism, including ammonium transporters (AMT), urea transporters (UT), nitrilase (NIT), phosphate transporters (PTA), alkaline phosphatase (PHOA), ferredoxin (FDX), flavodoxin (FldA) and nitrate reductase (NAR) (Supplementary Information 3.2). b, Genes encoding calcium EF hand (CaEF) proteins and others that bind metals such as copper, zinc and iron (Supplementary Information 3.2).

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Referenced accessions

Sequence Read Archive

Change history

Corrected online 10 July 2013
Spelling of author J.N. was corrected.

References

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Author information

  1. These authors contributed equally to this work.

    • Joel B. Dacks,
    • Charles F. Delwiche,
    • Sonya T. Dyhrman,
    • Gernot Glöckner,
    • Uwe John,
    • Thomas Richards,
    • Alexandra Z. Worden &
    • Xiaoyu Zhang

Affiliations

  1. Department of Biological Sciences, California State University San Marcos, San Marcos, California 92096, USA

    • Betsy A. Read &
    • Analissa F. Sarno
  2. Alfred Wegener Institute Helmholtz Center for Polar and Marine Research (AWI), 27570 Bremerhaven, Germany

    • Jessica Kegel,
    • Stephan Frickenhaus,
    • Klaus Valentin &
    • Uwe John
  3. Department of Cell Biology, University of Alberta, Edmonton, Alberta T6G 2H7, Canada

    • Mary J. Klute,
    • Maria Aguilar,
    • Emily K. Herman &
    • Joel B. Dacks
  4. US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA

    • Alan Kuo,
    • Asaf Salamov,
    • Jeremy Shmutz &
    • Igor V. Grigoriev
  5. J. Craig Venter Institute, San Diego, California 92121, USA

    • Stephane C. Lefebvre
  6. Institut National de la Recherché Agronomique, Unité de Recherche en Génomique-Info, Versailles 78026, France

    • Florian Maumus
  7. Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany

    • Christoph Mayer
  8. Department of Animal Ecology, Evolution and Biodiversity, Ruhr-University, D-44801 Bochum, Germany

    • Christoph Mayer
  9. Cell Biology and Molecular Genetics and the Maryland Agricultural Experiment Station, University of Maryland, College Park, Maryland 20742, USA

    • John Miller &
    • Charles F. Delwiche
  10. Monterey Bay Aquarium Research Institute, Moss Landing, California 95039, USA

    • Adam Monier &
    • Alexandra Z. Worden
  11. Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK

    • Jeremy Young
  12. Structural and Genomic Information Laboratory, CNRS, Aix-Marseille University, Mediterranean Institute of Microbiology, Marseille FR3479, France

    • Jean-Michel Claverie &
    • Hiroyuki Ogata
  13. Biotechnology, Hochschule Bremerhaven, An der Karlstadt 8, 27568 Bremerhaven, Germany

    • Stephan Frickenhaus
  14. Department of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115, USA

    • Karina Gonzalez
  15. Department of Plant Systems Biology, VIB, Ghent University, 9052 Ghent, Belgium

    • Yao-Cheng Lin &
    • Yves Van de Peer
  16. Department of Biological Chemistry, Rothamsted Research, Harpenden AL5 2JQ, UK

    • Johnathan Napier
  17. HudsonAlpha Genome Sequencing Center, Huntsville, Alabama 35806, USA

    • Jeremy Shmutz
  18. Marine Biological Association of the UK, Plymouth PL12PB, UK

    • Declan Schroeder &
    • Glen Wheeler
  19. CNRS UMR 7144 and Université Pierre et Marie Curie, EPEP team, Station Biologique de Roscoff, 29682 Roscoff Cedex, France

    • Colomban de Vargas
  20. School of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK

    • Frederic Verret
  21. Departmento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

    • Peter von Dassow
  22. Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3DH, UK

    • Glen Wheeler
  23. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA

    • Sonya T. Dyhrman
  24. Department of Earth and Environmental Sciences and Lamont-Doherty Earth Observatory, Columbia University, Palisades, New York 10964, USA

    • Sonya T. Dyhrman
  25. Institute for Biochemistry I, Medical Faculty, University of Cologne, D-50931, Germany and Leibniz-Institute of Freshwater Ecology and Inland Fisheries, D-12587 Berlin, Germany

    • Gernot Glöckner
  26. Department of Zoology, Natural History Museum, London SW7 5BD, UK

    • Thomas Richards
  27. Department of Computer Science and Information Systems, California State University San Marcos, California 92096, USA

    • Xiaoyu Zhang
  28. J. Craig Venter Institute, San Diego, California 92121, USA.

    • Andrew E. Allen
  29. Environmental Biophysics and Molecular Ecology Group, Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, New Jersey 08901, USA.

    • Kay Bidle
  30. Joint Georgia Tech and Emory Department of Biomedical Engineering, School of Computational Science and Engineering, Georgia Tech, Atlanta, Georgia 30322, USA.

    • Mark Borodovsky &
    • Alexandre Lomsadze
  31. Department of Bioinformatics, Moscow Institute for Physics and Technology, Moscow 117303, Russia.

    • Mark Borodovsky
  32. Environmental and Evolutionary Genomics Section, Institut de Biologie de l’Ecole Normale Supérieure, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8197, Institut National de la Santé et de la Recherche Médicale U1024, Ecole Normale Supérieure, 75230 Paris Cedex 05, France.

    • Chris Bowler
  33. Marine Biological Association of the UK, Plymouth PL12PB, UK.

    • Colin Brownlee &
    • Luke Mackinder
  34. CNRS, UMR 7139, Laboratoire International Associé Dispersal and Adaptation in Marine Species, Station Biologique de Roscoff, Place Georges Teissier, BP74, 29682 Roscoff Cedex, France.

    • J. Mark Cock
  35. UPMC Université Paris 06, The Marine Plants and Biomolecules Laboratory, UMR 7139, Station Biologique de Roscoff, Place Georges Teissier, BP74, 29682 Roscoff Cedex, France.

    • J. Mark Cock
  36. University of Ostrava, Faculty of Science, Department of Biology and Ecology, Life Science Research Centre, 710 00 Ostrava, Czech Republic.

    • Marek Elias
  37. Division of Genetics, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts 02115, USA.

    • Vadim N. Gladyshev &
    • Alexei Lobanov
  38. Leibniz Institute for Age Research - Fritz Lipmann Institute, Beutenbergstraße 11, 07745 Jena, Germany.

    • Marco Groth
  39. Department of Genetics, Cell Biology & Anatomy, Bioinformatics and Systems Biology Core, University of Nebraska Medical Center, Omaha, Nebraska 68198, USA.

    • Chittibabu Guda
  40. Department of Computer Science and Information Systems, California State University San Marcos, San Marcos, California 92096, USA.

    • Ahmad Hadaegh
  41. Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California 93106, USA.

    • Maria Debora Iglesias-Rodriguez
  42. Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO17 1BJ, UK.

    • Maria Debora Iglesias-Rodriguez,
    • Bethan M. Jones &
    • Sophie Richier
  43. HudsonAlpha Genome Sequencing Center, Huntsville, Alabama 35806, USA.

    • Jerry Jenkins
  44. Department of Microbiology, Oregon State University, Corvallis, Oregon 97331, USA.

    • Bethan M. Jones
  45. School of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK.

    • Tracy Lawson &
    • Christine Raines
  46. Department of Animal Ecology, Evolution and Biodiversity, Ruhr-University D-44801 Bochum, Germany.

    • Florian Leese
  47. US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.

    • Erika Lindquist
  48. Canadian Institute for Advanced Research Program in Integrated Microbial Biodiversity, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.

    • Shehre-Banoo Malik
  49. University of Texas-Houston Medical School, Houston, Texas 77030, USA.

    • Mary E. Marsh
  50. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR47TJ, UK.

    • Thomas Mock
  51. University of Potsdam, Institute of Biochemistry and Biology, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany.

  52. Department of Biology, University of Bergen, Thormøhlensgate 53 A & B, N-5006 Bergen, Norway.

    • António Pagarete
  53. Center for Environmental Genomics, PNW Center for Human Health and Ocean Studies, University of Washington, Seattle, Washington 98195-7940, USA.

    • Micaela Parker
  54. CNRS UMR 7144 and Université Pierre et Marie Curie, EPEP team, Station Biologique de Roscoff, 29682 Roscoff Cedex, France.

  55. Institut National de la Recherché Agronomique, Unité de Recherche en Génomique-Info, Versailles 78026, France.

    • Hadi Quesneville
  56. Faculty of Biology and BIOSS Centre for Biological Signalling Studies, University of Freiburg, Friedrichstrasse 39, 79098 Freiburg, Germany.

    • Stefan A. Rensing
  57. Faculty of Biology, University of Marburg, Karl-von-Frisch-Strasse 8, 35043 Marburg, Germany.

    • Stefan A. Rensing
  58. Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá Distrito Capital, 111711, Colombia.

    • Diego Mauricio Riaño-Pachón
  59. INSU CNRS, Lab Oceanography Villefranche, UMR7093, F-06234 Villefranche Sur Mer, France.

    • Sophie Richier
  60. Université Paris 06, Observatoire Océanologique Villefranche, F-06230 Villefranche Sur Mer, France.

    • Sophie Richier
  61. Alfred Wegener Institute Helmholtz Center for Polar and Marine Research (AWI), 27570 Bremerhaven, Germany

  62. Faculty of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba Ibaraki Prefecture 305-8572, Japan.

    • Yoshihiro Shiraiwa
  63. Biosciences, College of Life & Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK.

    • Darren M. Soanes,
    • Mark van der Giezen &
    • Bryony Williams
  64. Department of Biological Sciences, California State University San Marcos, San Marcos, California 92096, USA.

    • Thomas M. Wahlund
  65. Provasoli-Guillard National Center for Marine Algae and Microbiota, Bigelow Laboratory for Ocean Sciences, 60 Bigelow Way, East Boothbay, Maine 04544, USA.

    • Willie Wilson
  66. Department of Biological Sciences, California State University Chico, 1205 West 7th Street, Chico, California 95929-0515, USA.

    • Gordon Wolfe
  67. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA.

    • Louie L. Wurch
  68. Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA.

    • Louie L. Wurch

Consortia

  1. Emiliania huxleyi Annotation Consortium

    • Andrew E. Allen,
    • Kay Bidle,
    • Mark Borodovsky,
    • Chris Bowler,
    • Colin Brownlee,
    • J. Mark Cock,
    • Marek Elias,
    • Vadim N. Gladyshev,
    • Marco Groth,
    • Chittibabu Guda,
    • Ahmad Hadaegh,
    • Maria Debora Iglesias-Rodriguez,
    • Jerry Jenkins,
    • Bethan M. Jones,
    • Tracy Lawson,
    • Florian Leese,
    • Erika Lindquist,
    • Alexei Lobanov,
    • Alexandre Lomsadze,
    • Shehre-Banoo Malik,
    • Mary E. Marsh,
    • Luke Mackinder,
    • Thomas Mock,
    • Bernd Mueller-Roeber,
    • António Pagarete,
    • Micaela Parker,
    • Ian Probert,
    • Hadi Quesneville,
    • Christine Raines,
    • Stefan A. Rensing,
    • Diego Mauricio Riaño-Pachón,
    • Sophie Richier,
    • Sebastian Rokitta,
    • Yoshihiro Shiraiwa,
    • Darren M. Soanes,
    • Mark van der Giezen,
    • Thomas M. Wahlund,
    • Bryony Williams,
    • Willie Wilson,
    • Gordon Wolfe &
    • Louie L. Wurch

Contributions

Genome sequencing was performed by the US DOE JGI. B.A.R. coordinated the project and I.V.G. coordinated JGI sequencing/analysis; J.S. performed assemblies; A.K. and A.S. conducted automated annotation and analysis; U.J. at the AWI performed Illumina sequencing of 13 additional strains; A.K., X.Z., U.J., G.G., F.M., C.d.V., S.F., C.M., H.O., F.V., D.S., S.C.L., A.M., J.-M.C., Y.-C.L., Y.V.d.P., J.K., K.V., K.G., A.F.S., J.N., P.v.D. and G.W. performed genome and transcriptome analyses; U.J. and G.G. provided Illumina genomic sequence data, F.V. and D.S., tiling array data, and J. K., microarray data; J.Y. provided SEM images; phylogenetic anaylses was contributed by A.M., and A.Z.W. (Fig. 1b); E.K.H., M.J.K. and J.B.D. (Fig. 3c); J.M., C.F.D., M.A. U.J., and J.B.D (Supplementary Fig. 1); B.A.R. wrote the manuscript in collaboration with J.B.D., C.F.D., S.T.D., G.G., U.J., T.R., A.Z.W, X.Z. and I.V.G. (co-second senior authors). Authors in the first alphabetical list of the paper are equally contributing second authors who made substantial contributions to the paper. The remaining authors are members of the E. huxleyi Annotation Consortium who contributed additional analyses and/or annotations.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

This paper is distributed under the terms of the Creative Commons Attribution-Non-Commercial-Share Alike licence, and the online version of this paper is freely available to all readers. Assembly and annotation data for E. huxleyi strain 1516 are available through JGI Genome Portal at http://jgi.doe.gov/Ehux and at DDBJ/EMBL/GenBank under accession number AHAL00000000. The version described in this paper is the first version, AHAL01000000. Sequence information for other strains can be found at the Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) under the accession number SRA048733.2.

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Supplementary information

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  1. Supplementary Information (3 MB)

    This file contains Supplementary Text and Data in 5 sections – see contents for details.

  2. Supplementary Information (478 KB)

    This file contains Supplementary Figures 1-6 and Supplementary Tables 1-15.

Excel files

  1. Supplementary Data 1 (765 KB)

    This file contains refined gene models validated by Sanger ESTs.

  2. Supplementary Data 2 (210 KB)

    This file contains refined gene models validated by tiling arrays.

  3. Supplementary Data 3 (236 KB)

    This file contains refined gene models validated by RNAseq.

  4. Supplementary Data 4 (230 KB)

    This file contains a phylogenomic gene list.

  5. Supplementary Data 5 (384 KB)

    This file contains core and variable genes identified by direct mapping of Illumina reads based on 50% gene coverage.

  6. Supplementary Data 6 (643 KB)

    This file contains core genes identified by comparative genomic hybridization.

  7. Supplementary Data 7 (64 KB)

    This file contains conserved eukaryotic genes mapping approach (CEGMA) list.

  8. Supplementary Data 8 (50 KB)

    This file contains genes encoding putative metal binding proteins.

Additional data