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The ctenophore genome and the evolutionary origins of neural systems

Author

Listed:
  • Leonid L. Moroz

    (The Whitney Laboratory for Marine Bioscience, University of Florida
    University of Florida
    Friday Harbor Laboratories, University of Washington)

  • Kevin M. Kocot

    (Auburn University, 101 Rouse Life Sciences, Auburn, Alabama 36849, USA)

  • Mathew R. Citarella

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Sohn Dosung

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Tigran P. Norekian

    (The Whitney Laboratory for Marine Bioscience, University of Florida
    Friday Harbor Laboratories, University of Washington)

  • Inna S. Povolotskaya

    (Centre for Genomic Regulation (CRG)
    Universitat Pompeu Fabra (UPF))

  • Anastasia P. Grigorenko

    (Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School
    Vavilov Institute of General Genetics, Russian Academy of Sciences (RAS))

  • Christopher Dailey

    (University of Illinois Urbana-Champaign)

  • Eugene Berezikov

    (European Research Institute for the Biology of Ageing, University of Groningen Medical Center)

  • Katherine M. Buckley

    (University of Toronto, Sunnybrook Research Institute 2075 Bayview Avenue)

  • Andrey Ptitsyn

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Denis Reshetov

    (Vavilov Institute of General Genetics, Russian Academy of Sciences (RAS))

  • Krishanu Mukherjee

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Tatiana P. Moroz

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Yelena Bobkova

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Fahong Yu

    (University of Florida)

  • Vladimir V. Kapitonov

    (Genetic Information Research Institute, 1925 Landings Dr.)

  • Jerzy Jurka

    (Genetic Information Research Institute, 1925 Landings Dr.)

  • Yuri V. Bobkov

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Joshua J. Swore

    (The Whitney Laboratory for Marine Bioscience, University of Florida
    Friday Harbor Laboratories, University of Washington)

  • David O. Girardo

    (The Whitney Laboratory for Marine Bioscience, University of Florida
    Friday Harbor Laboratories, University of Washington)

  • Alexander Fodor

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Fedor Gusev

    (Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School
    Vavilov Institute of General Genetics, Russian Academy of Sciences (RAS))

  • Rachel Sanford

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

  • Rebecca Bruders

    (The Whitney Laboratory for Marine Bioscience, University of Florida
    Friday Harbor Laboratories, University of Washington)

  • Ellen Kittler

    (Program in Molecular Medicine, University of Massachusetts Medical School)

  • Claudia E. Mills

    (Friday Harbor Laboratories, University of Washington)

  • Jonathan P. Rast

    (University of Toronto, Sunnybrook Research Institute 2075 Bayview Avenue)

  • Romain Derelle

    (Centre for Genomic Regulation (CRG)
    Universitat Pompeu Fabra (UPF))

  • Victor V. Solovyev

    (Royal Holloway, University of London)

  • Fyodor A. Kondrashov

    (Centre for Genomic Regulation (CRG)
    Universitat Pompeu Fabra (UPF)
    Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluis Companys 23)

  • Billie J. Swalla

    (Friday Harbor Laboratories, University of Washington)

  • Jonathan V. Sweedler

    (University of Illinois Urbana-Champaign)

  • Evgeny I. Rogaev

    (Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School
    Vavilov Institute of General Genetics, Russian Academy of Sciences (RAS)
    Center for Brain Neurobiology and Neurogenetics and Institute of Cytology and Genetics, RAS
    Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University)

  • Kenneth M. Halanych

    (Auburn University, 101 Rouse Life Sciences, Auburn, Alabama 36849, USA)

  • Andrea B. Kohn

    (The Whitney Laboratory for Marine Bioscience, University of Florida)

Abstract

The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores (comb jellies) have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes, and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well recognized in ctenophores, many bilaterian neuron-specific genes and genes of ‘classical’ neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.

Suggested Citation

  • Leonid L. Moroz & Kevin M. Kocot & Mathew R. Citarella & Sohn Dosung & Tigran P. Norekian & Inna S. Povolotskaya & Anastasia P. Grigorenko & Christopher Dailey & Eugene Berezikov & Katherine M. Buckle, 2014. "The ctenophore genome and the evolutionary origins of neural systems," Nature, Nature, vol. 510(7503), pages 109-114, June.
  • Handle: RePEc:nat:nature:v:510:y:2014:i:7503:d:10.1038_nature13400
    DOI: 10.1038/nature13400
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    Cited by:

    1. Minjun Jin & Wanqing Li & Zhongyu Ji & Guotao Di & Meng Yuan & Yifan Zhang & Yunsi Kang & Chengtian Zhao, 2024. "Coordinated cellular behavior regulated by epinephrine neurotransmitters in the nerveless placozoa," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. 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.
    3. 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.

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