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.

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.

Metrics

  • 6,101
    views
  • 671
    downloads
  • 102
    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. 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

Further reading

    1. Computational and Systems Biology
    2. Evolutionary Biology
    Pierre Barrat-Charlaix, Richard A Neher
    Research Article

    As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.

    1. Ecology
    2. Evolutionary Biology
    Rebecca D Tarvin, Jeffrey L Coleman ... Richard W Fitch
    Research Article

    Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.