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The Amphimedon queenslandica genome and the evolution of animal complexity

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  • Mansi Srivastava

    (University of California
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Oleg Simakov

    (Molecular Evolution Genomics, University of Heidelberg, 69117 Heidelberg, Germany
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Jarrod Chapman

    (Department of Energy Joint Genome Institute)

  • Bryony Fahey

    (School of Biological Sciences, The University of Queensland)

  • Marie E. A. Gauthier

    (School of Biological Sciences, The University of Queensland
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Therese Mitros

    (University of California)

  • Gemma S. Richards

    (School of Biological Sciences, The University of Queensland
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Cecilia Conaco

    (Neuroscience Research Institute, University of California Santa Barbara)

  • Michael Dacre

    (Razavi Newman Center for Bioinformatics, Salk Institute for Biological Studies)

  • Uffe Hellsten

    (Department of Energy Joint Genome Institute)

  • Claire Larroux

    (School of Biological Sciences, The University of Queensland
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Nicholas H. Putnam

    (Rice University, 6100 Main Street, Houston, Texas 77005, USA)

  • Mario Stanke

    (Institut für Mikrobiologie und Genetik, Goldschmidtstr. 1, 37077 Göttingen, Germany)

  • Maja Adamska

    (School of Biological Sciences, The University of Queensland
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Aaron Darling

    (Genome Center, University of California-Davis)

  • Sandie M. Degnan

    (School of Biological Sciences, The University of Queensland)

  • Todd H. Oakley

    (Evolution and Marine Biology, University of California Santa Barbara)

  • David C. Plachetzki

    (Evolution and Marine Biology, University of California Santa Barbara)

  • Yufeng Zhai

    (Razavi Newman Center for Bioinformatics, Salk Institute for Biological Studies)

  • Marcin Adamski

    (School of Biological Sciences, The University of Queensland
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Andrew Calcino

    (School of Biological Sciences, The University of Queensland)

  • Scott F. Cummins

    (School of Biological Sciences, The University of Queensland)

  • David M. Goodstein

    (Department of Energy Joint Genome Institute)

  • Christina Harris

    (School of Biological Sciences, The University of Queensland)

  • Daniel J. Jackson

    (School of Biological Sciences, The University of Queensland
    Present addresses: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02138, USA (M.Sr.); EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany (O.S.); Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstr. 190, CH-8057 Zurich, Switzerland (M.E.A.G.); Sars International Centre for Marine Molecular Biology, N-5008 Bergen, Norway (G.S.R., Maj.A., Mar.A.); Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-University, 80333 Munich, Germany (C.L.); Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstr.3, 37077 Göttingen, Germany (D.J.J.).)

  • Sally P. Leys

    (University of Alberta)

  • Shengqiang Shu

    (Department of Energy Joint Genome Institute)

  • Ben J. Woodcroft

    (School of Biological Sciences, The University of Queensland)

  • Michel Vervoort

    (Development and Neurobiology program Institut Jacques Monod, UMR 7592 CNRS/Université Paris Diderot-Paris 7, 75205 Paris Cedex 13, France)

  • Kenneth S. Kosik

    (Neuroscience Research Institute, University of California Santa Barbara)

  • Gerard Manning

    (Razavi Newman Center for Bioinformatics, Salk Institute for Biological Studies)

  • Bernard M. Degnan

    (School of Biological Sciences, The University of Queensland)

  • Daniel S. Rokhsar

    (University of California
    Department of Energy Joint Genome Institute)

Abstract

Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse ‘toolkit’ of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.

Suggested Citation

  • Mansi Srivastava & Oleg Simakov & Jarrod Chapman & Bryony Fahey & Marie E. A. Gauthier & Therese Mitros & Gemma S. Richards & Cecilia Conaco & Michael Dacre & Uffe Hellsten & Claire Larroux & Nicholas, 2010. "The Amphimedon queenslandica genome and the evolution of animal complexity," Nature, Nature, vol. 466(7307), pages 720-726, August.
    • Handle: RePEc:nat:nature:v:466:y:2010:i:7307:d:10.1038_nature09201
    DOI: 10.1038/nature09201
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    Cited by:

    1. Joan Gizzio & Abhishek Thakur & Allan Haldane & Carol Beth Post & Ronald M. Levy, 2024. "Evolutionary sequence and structural basis for the distinct conformational landscapes of Tyr and Ser/Thr kinases," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Bob Zimmermann & Juan D. Montenegro & Sofia M. C. Robb & Whitney J. Fropf & Lukas Weilguny & Shuonan He & Shiyuan Chen & Jessica Lovegrove-Walsh & Eric M. Hill & Cheng-Yi Chen & Katerina Ragkousi & Da, 2023. "Topological structures and syntenic conservation in sea anemone genomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Christine Guzman & Kurato Mohri & Ryotaro Nakamura & Minato Miyake & Yuko Tsuchiya & Kentaro Tomii & Hiroshi Watanabe, 2024. "Neuronal and non-neuronal functions of the synaptic cell adhesion molecule neurexin in Nematostella vectensis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Lauren E. Vandepas & Caroline Stefani & Phillip P. Domeier & Nikki Traylor-Knowles & Frederick W. Goetz & William E. Browne & Adam Lacy-Hulbert, 2024. "Extracellular DNA traps in a ctenophore demonstrate immune cell behaviors in a non-bilaterian," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    5. Kriti Shah & Shiyang He & David J. Turner & Joshua Corbo & Khadija Rebbani & Daniel Dominguez & Joseph M. Bateman & Sihem Cheloufi & Cátia Igreja & Eugene Valkov & Jernej Murn, 2024. "Regulation by the RNA-binding protein Unkempt at its effector interface," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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