Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles

  1. Jan Janouškovec  Is a corresponding author
  2. Gita G Paskerova
  3. Tatiana S Miroliubova
  4. Kirill V Mikhailov
  5. Thomas Birley
  6. Vladimir V Aleoshin
  7. Timur G Simdyanov
  1. University College London, United Kingdom
  2. Saint Petersburg State University, Russian Federation
  3. Lomonosov Moscow State University, Russian Federation

Abstract

The phylum Apicomplexa comprises human pathogens such as Plasmodium but are also an under-explored hotspot of evolutionary diversity central to understanding the origins of parasitism and non-photosynthetic plastids. We generated single-cell transcriptomes for all major apicomplexan groups lacking large-scale sequence data. Phylogenetic analysis reveals that apicomplexan-like parasites are polyphyletic and their similar morphologies emerged convergently at least three times. Gregarines and eugregarines are monophyletic, against most expectations, and rhytidocystids and Eleutheroschizon are sister lineages to medically important taxa. Although previously unrecognized, plastids in deep-branching apicomplexans are common, and they contain some of the most divergent and AT-rich genomes ever found. In eugregarines, however, plastids are either abnormally reduced or absent, thus increasing known plastid losses in eukaryotes from two to four. Environmental sequences of ten novel plastid lineages and structural innovations in plastid proteins confirm that plastids in apicomplexans and their relatives are widespread and share a common, photosynthetic origin.

Data availability

Sequence data have been deposited in NCBI under the Bioproject accessions PRJNA557242 and PRJNA556465. Sources of data for individual analyses are provided in Supplemental Tables S1 to S7.

The following data sets were generated

Article and author information

Author details

  1. Jan Janouškovec

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    For correspondence
    janjan.cz@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6547-749X
  2. Gita G Paskerova

    Department of Invertebrate Zoology, Saint Petersburg State University, St Petersburg, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1026-4216
  3. Tatiana S Miroliubova

    Department of Invertebrate Zoology, Saint Petersburg State University, St Petersburg, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  4. Kirill V Mikhailov

    Belozersky Institute for Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  5. Thomas Birley

    Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Vladimir V Aleoshin

    Belozersky Institute for Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3299-9950
  7. Timur G Simdyanov

    Faculty of Biology, Lomonosov Moscow State University, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2478-9301

Funding

University College London (Excellence Research Fellowship)

  • Jan Janouškovec

Russian Foundation for Basic Research (18-04-00324)

  • Gita G Paskerova
  • Timur G Simdyanov

Russian Science Foundation (18-04-00123)

  • Vladimir V Aleoshin

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

Reviewing Editor

  1. John McCutcheon, University of Montana

Version history

  1. Received: June 25, 2019
  2. Accepted: August 14, 2019
  3. Accepted Manuscript published: August 16, 2019 (version 1)
  4. Version of Record published: September 9, 2019 (version 2)
  5. Version of Record updated: September 10, 2019 (version 3)

Copyright

© 2019, Janouškovec 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. Jan Janouškovec
  2. Gita G Paskerova
  3. Tatiana S Miroliubova
  4. Kirill V Mikhailov
  5. Thomas Birley
  6. Vladimir V Aleoshin
  7. Timur G Simdyanov
(2019)
Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles
eLife 8:e49662.
https://doi.org/10.7554/eLife.49662

Share this article

https://doi.org/10.7554/eLife.49662

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