1. Cell Biology
  2. Evolutionary Biology
Download icon

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
Research Article
  • Cited 60
  • Views 2,298
  • Annotations
Cite this article as: eLife 2017;6:e23717 doi: 10.7554/eLife.23717

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.

Data availability

The following data sets were generated

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

Publication 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.

Metrics

  • 2,298
    Page views
  • 549
    Downloads
  • 60
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Cell Biology
    2. Medicine
    Srinu Tumpara et al.
    Short Report

    The CX3CR1 (chemokine (C-X3-C motif) receptor 1) expression levels on immune cells have significant importance in maintaining tissue homeostasis under physiological and pathological conditions. The factors implicated in the regulation of CX3CR1 and its specific ligand CX3CL1 (fractalkine) expression remain largely unknown. Recent studies provide evidence that host`s misfolded proteins occurring in the forms of polymers or amyloid fibrils can regulate CX3CR1 expression. Herein, a novel example demonstrates that polymers of human ZZ alpha-1 antitrypsin (Z-AAT) protein, resulting from its conformational misfolding due to the Z (Glu342Lys) mutation in SERPINA1 gene, strongly lower CX3CR1 mRNA expression in human PBMCs. This parallels with increase of intracellular levels of CX3CR1 and Z-AAT proteins. Presented data indicate the involvement of the CX3CR1 pathway in the Z-AAT-related disorders and further support the role of misfolded proteins in CX3CR1 regulation.

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Michael Chas Sumner et al.
    Research Article

    Hundreds of genes interact with the yeast nuclear pore complex (NPC), localizing at the nuclear periphery and clustering with co-regulated genes. Dynamic tracking of peripheral genes shows that they cycle on and off the NPC and that interaction with the NPC slows their sub-diffusive movement. Furthermore, NPC-dependent inter-chromosomal clustering leads to coordinated movement of pairs of loci separated by hundreds of nanometers. We developed Fractional Brownian Motion simulations for chromosomal loci in the nucleoplasm and interacting with NPCs. These simulations predict the rate and nature of random sub-diffusion during repositioning from nucleoplasm to periphery and match measurements from two different experimental models, arguing that recruitment to the nuclear periphery is due to random sub-diffusion and transient capture by NPCs. Finally, the simulations do not lead to inter-chromosomal clustering or coordinated movement, suggesting that interaction with the NPC is necessary, but not sufficient, to cause clustering.