Insights into early animal evolution form the genome of the xenacoelomorph worm Xenoturbella bocki

  1. Philipp H Schiffer  Is a corresponding author
  2. Paschalis Natsidis
  3. Daniel J Leite
  4. Helen E Robertson
  5. François Lapraz
  6. Ferdinand Marlétaz
  7. Bastian Fromm
  8. Liam Baudry
  9. Fraser Simpson
  10. Eirik Høye
  11. Anne C Zakrzewski
  12. ‪Paschalia Kapli
  13. Katharina J Hoff
  14. Steven Mueller
  15. Martial Marbouty
  16. Heather Marlow
  17. Richard R Copley
  18. Romain Koszul
  19. Peter Sarkies
  20. Maximilian J Telford  Is a corresponding author
  1. University of Cologne, Germany
  2. University College London, United Kingdom
  3. Durham University, United Kingdom
  4. Université Côte d'Azur, France
  5. UiT The Arctic University of Norway, Norway
  6. Institut Pasteur, France
  7. University of Greifswald, Germany
  8. University of Chicago, United States
  9. Sorbonne Université, France
  10. University of Oxford, United Kingdom

Abstract

The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help to understand the evolution and biology of enigmatic species better. Here we assemble and analyse the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome like scaffolds, with repeat content and intron, exon and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.

Data availability

All read sets (RNA and DNA derived) used in this study will be made available with the publication of this manuscript on the SRA database under the BioProject ID PRJNA864813. Hi-C reads are deposited under SAMN30224387, RNA-Seq under SAMN35083895. The genome assemblies of X. bocki (ERS12565994, ERA16814408) and the Chlamydia sp. (ERS12566084, ERA16814775) are deposited under PRJEB55230 at ENA.Supplementary online material (described in the manuscript) has be made available on Zenodo: doi:10.5281/zenodo.6962271

The following data sets were generated

Article and author information

Author details

  1. Philipp H Schiffer

    Institute of Zoology, University of Cologne, Köln, Germany
    For correspondence
    philipp.schiffer@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6776-0934
  2. Paschalis Natsidis

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel J Leite

    Department of Biosciences, Durham University, Durham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9966-4760
  4. Helen E Robertson

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. François Lapraz

    Université Côte d'Azur, Nice, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9209-2018
  6. Ferdinand Marlétaz

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Bastian Fromm

    UiT The Arctic University of Norway, Tromsø, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0352-3037
  8. Liam Baudry

    Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Fraser Simpson

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Eirik Høye

    UiT The Arctic University of Norway, Tromsø, Norway
    Competing interests
    The authors declare that no competing interests exist.
  11. Anne C Zakrzewski

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. ‪Paschalia Kapli

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. Katharina J Hoff

    Institute for Mathematics and Computer Science, University of Greifswald, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Steven Mueller

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  15. Martial Marbouty

    Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1668-8423
  16. Heather Marlow

    Division of Biological Sciences, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Richard R Copley

    Laboratoire de Biologie du Dé veloppement de Villefranche-sur-mer, Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  18. Romain Koszul

    Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3086-1173
  19. Peter Sarkies

    Department of Biochemistry, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0279-6199
  20. Maximilian J Telford

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    For correspondence
    m.telford@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3749-5620

Funding

European Research Council (ERC-2012-AdG 322790)

  • Philipp H Schiffer
  • Helen E Robertson
  • Anne C Zakrzewski
  • Steven Mueller
  • Maximilian J Telford

Deutsche Forschungsgemeinschaft (434028868)

  • Philipp H Schiffer

Biotechnology and Biological Sciences Research Council (BB/R016240/1)

  • Paschalis Natsidis
  • Maximilian J Telford

Leverhulme Trust (RPG-2018-302)

  • Daniel J Leite
  • Maximilian J Telford

HORIZON EUROPE Marie Sklodowska-Curie Actions (764840 IGNITE)

  • Paschalis Natsidis
  • Maximilian J Telford

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2024, Schiffer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Philipp H Schiffer
  2. Paschalis Natsidis
  3. Daniel J Leite
  4. Helen E Robertson
  5. François Lapraz
  6. Ferdinand Marlétaz
  7. Bastian Fromm
  8. Liam Baudry
  9. Fraser Simpson
  10. Eirik Høye
  11. Anne C Zakrzewski
  12. ‪Paschalia Kapli
  13. Katharina J Hoff
  14. Steven Mueller
  15. Martial Marbouty
  16. Heather Marlow
  17. Richard R Copley
  18. Romain Koszul
  19. Peter Sarkies
  20. Maximilian J Telford
(2024)
Insights into early animal evolution form the genome of the xenacoelomorph worm Xenoturbella bocki
eLife 13:e94948.
https://doi.org/10.7554/eLife.94948

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https://doi.org/10.7554/eLife.94948

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