1. Cell Biology
  2. Evolutionary Biology

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
https://doi.org/10.7554/eLife.23717
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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

  • 3,217
    views
  • 681
    downloads
  • 128
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  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

Categories and tags

Further reading

    1. Cell Biology
    2. Computational and Systems Biology

    Unbiased identification of cell identity in dense mixed neural cultures

    Sarah De Beuckeleer, Tim Van De Looverbosch ... Winnok H De Vos
    Research Article

    Induced pluripotent stem cell (iPSC) technology is revolutionizing cell biology. However, the variability between individual iPSC lines and the lack of efficient technology to comprehensively characterize iPSC-derived cell types hinder its adoption in routine preclinical screening settings. To facilitate the validation of iPSC-derived cell culture composition, we have implemented an imaging assay based on cell painting and convolutional neural networks to recognize cell types in dense and mixed cultures with high fidelity. We have benchmarked our approach using pure and mixed cultures of neuroblastoma and astrocytoma cell lines and attained a classification accuracy above 96%. Through iterative data erosion, we found that inputs containing the nuclear region of interest and its close environment, allow achieving equally high classification accuracy as inputs containing the whole cell for semi-confluent cultures and preserved prediction accuracy even in very dense cultures. We then applied this regionally restricted cell profiling approach to evaluate the differentiation status of iPSC-derived neural cultures, by determining the ratio of postmitotic neurons and neural progenitors. We found that the cell-based prediction significantly outperformed an approach in which the population-level time in culture was used as a classification criterion (96% vs 86%, respectively). In mixed iPSC-derived neuronal cultures, microglia could be unequivocally discriminated from neurons, regardless of their reactivity state, and a tiered strategy allowed for further distinguishing activated from non-activated cell states, albeit with lower accuracy. Thus, morphological single-cell profiling provides a means to quantify cell composition in complex mixed neural cultures and holds promise for use in the quality control of iPSC-derived cell culture models.

    1. Cell Biology

    Endocytic recycling is central to circadian collagen fibrillogenesis and disrupted in fibrosis

    Joan Chang, Adam Pickard ... Karl E Kadler
    Research Article

    Collagen-I fibrillogenesis is crucial to health and development, where dysregulation is a hallmark of fibroproliferative diseases. Here, we show that collagen-I fibril assembly required a functional endocytic system that recycles collagen-I to assemble new fibrils. Endogenous collagen production was not required for fibrillogenesis if exogenous collagen was available, but the circadian-regulated vacuolar protein sorting (VPS) 33b and collagen-binding integrin α11 subunit were crucial to fibrillogenesis. Cells lacking VPS33B secrete soluble collagen-I protomers but were deficient in fibril formation, thus secretion and assembly are separately controlled. Overexpression of VPS33B led to loss of fibril rhythmicity and overabundance of fibrils, which was mediated through integrin α11β1. Endocytic recycling of collagen-I was enhanced in human fibroblasts isolated from idiopathic pulmonary fibrosis, where VPS33B and integrin α11 subunit were overexpressed at the fibrogenic front; this correlation between VPS33B, integrin α11 subunit, and abnormal collagen deposition was also observed in samples from patients with chronic skin wounds. In conclusion, our study showed that circadian-regulated endocytic recycling is central to homeostatic assembly of collagen fibrils and is disrupted in diseases.

    1. Cell Biology

    Hypersensitive intercellular responses of endometrial stromal cells drive invasion in endometriosis

    Chun-Wei Chen, Jeffery B Chavez ... Bruce J Nicholson
    Research Article Updated

    Endometriosis is a debilitating disease affecting 190 million women worldwide and the greatest single contributor to infertility. The most broadly accepted etiology is that uterine endometrial cells retrogradely enter the peritoneum during menses, and implant and form invasive lesions in a process analogous to cancer metastasis. However, over 90% of women suffer retrograde menstruation, but only 10% develop endometriosis, and debate continues as to whether the underlying defect is endometrial or peritoneal. Processes implicated in invasion include: enhanced motility; adhesion to, and formation of gap junctions with, the target tissue. Endometrial stromal (ESCs) from 22 endometriosis patients at different disease stages show much greater invasiveness across mesothelial (or endothelial) monolayers than ESCs from 22 control subjects, which is further enhanced by the presence of EECs. This is due to the enhanced responsiveness of endometriosis ESCs to the mesothelium, which induces migration and gap junction coupling. ESC-PMC gap junction coupling is shown to be required for invasion, while coupling between PMCs enhances mesothelial barrier breakdown.