Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome

  1. Richard G Dorrell  Is a corresponding author
  2. Gillian Gile
  3. Giselle McCallum
  4. Raphaël Méheust
  5. Eric P Bapteste
  6. Christen M Klinger
  7. Loraine Brillet-Guéguen
  8. Katalina D Freeman
  9. Daniel J Richter
  10. Chris Bowler
  1. École Normale Supérieure, CNRS, Inserm, PSL Research University, France
  2. Arizona State University, United States
  3. Université Pierre et Marie Curie, France
  4. University of Alberta, Canada
  5. CNRS, UPMC, FR2424, ABiMS, Station Biologique, France
  6. Sorbonne Universités, UPMC Univ Paris 06, CNRS UMR 7144, France

Abstract

Plastids are supported by a wide range of proteins encoded within the nucleus and imported from the cytoplasm. These plastid-targeted proteins may originate from the endosymbiont, the host, or other sources entirely. Here, we identify and characterise 770 plastid-targeted proteins that are conserved across the ochrophytes, a major group of algae including diatoms, pelagophytes and kelps, that possess plastids derived from red algae. We show that the ancestral ochrophyte plastid proteome was an evolutionary chimera, with 25% of its phylogenetically tractable proteins deriving from green algae. We additionally show that functional mixing of host and plastid proteomes, such as through dual targeting, is an ancestral feature of plastid evolution. Finally, we detect a clear phylogenetic signal from one ochrophyte subgroup, the lineage containing pelagophytes and dictyochophytes, in plastid-targeted proteins from another major algal lineage, the haptophytes. This may represent a possible serial endosymbiosis event deep in eukaryotic evolutionary history.

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Article and author information

Author details

  1. Richard G Dorrell

    IBENS, Département de Biologie, École Normale Supérieure, CNRS, Inserm, PSL Research University, Paris, France
    For correspondence
    dorrell@biologie.ens.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6263-9115
  2. Gillian Gile

    School of Life Sciences, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Giselle McCallum

    IBENS, Département de Biologie, École Normale Supérieure, CNRS, Inserm, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Raphaël Méheust

    Institut de Biologie Paris-Seine, Université Pierre et Marie Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4847-426X
  5. Eric P Bapteste

    Institut de Biologie Paris-Seine, Université Pierre et Marie Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Christen M Klinger

    Department of Cell Biology, University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Loraine Brillet-Guéguen

    CNRS, UPMC, FR2424, ABiMS, Station Biologique, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Katalina D Freeman

    School of Life Sciences, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Daniel J Richter

    Adaptation et Diversité en Milieu Marin, Sorbonne Universités, UPMC Univ Paris 06, CNRS UMR 7144, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9238-5571
  10. Chris Bowler

    IBENS, Département de Biologie, École Normale Supérieure, CNRS, Inserm, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

EMBO (ALTF 1124/2014)

  • Richard G Dorrell

ERC (Diatomite)

  • Chris Bowler

LouisD Foundation

  • Chris Bowler

FP7 (615274)

  • Eric P Bapteste

Gordon and Betty Moore Foundation

  • Chris Bowler

MEMO-LIFE (ANR- 10-LABX-54)

  • Chris Bowler

ANR (ANR-11-IDEX-0001-02)

  • Chris Bowler

ANR (ANR-11-BTBR-0008)

  • Daniel J Richter

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

Reviewing Editor

  1. Debashish Bhattacharya, Rutgers University, United States

Version history

  1. Received: November 28, 2016
  2. Accepted: May 8, 2017
  3. Accepted Manuscript published: May 12, 2017 (version 1)
  4. Version of Record published: June 7, 2017 (version 2)

Copyright

© 2017, Dorrell 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. Richard G Dorrell
  2. Gillian Gile
  3. Giselle McCallum
  4. Raphaël Méheust
  5. Eric P Bapteste
  6. Christen M Klinger
  7. Loraine Brillet-Guéguen
  8. Katalina D Freeman
  9. Daniel J Richter
  10. Chris Bowler
(2017)
Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome
eLife 6:e23717.
https://doi.org/10.7554/eLife.23717

Share this article

https://doi.org/10.7554/eLife.23717

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