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Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae

Author

Listed:
  • Max E. Schön

    (Uppsala University
    Uppsala University)

  • Vasily V. Zlatogursky

    (Uppsala University
    St. Petersburg State University)

  • Rohan P. Singh

    (Arizona State University)

  • Camille Poirier

    (GEOMAR Helmholtz Centre for Ocean Research Kiel
    Monterey Bay Aquarium Research Institute
    University of Oxford)

  • Susanne Wilken

    (Monterey Bay Aquarium Research Institute
    University of Amsterdam)

  • Varsha Mathur

    (University of British Columbia)

  • Jürgen F. H. Strassert

    (Uppsala University
    Leibniz Institute of Freshwater Ecology and Inland Fisheries)

  • Jarone Pinhassi

    (Linnaeus University)

  • Alexandra Z. Worden

    (GEOMAR Helmholtz Centre for Ocean Research Kiel
    Monterey Bay Aquarium Research Institute)

  • Patrick J. Keeling

    (University of British Columbia)

  • Thijs J. G. Ettema

    (Wageningen University and Research)

  • Jeremy G. Wideman

    (Arizona State University)

  • Fabien Burki

    (Uppsala University
    Uppsala University)

Abstract

The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in members of the eukaryotic supergroup Archaeplastida. All known archaeplastids still retain some form of primary plastids, which are widely assumed to have a single origin. Here, we use single-cell genomics from natural samples combined with phylogenomics to infer the evolutionary origin of the phylum Picozoa, a globally distributed but seemingly rare group of marine microbial heterotrophic eukaryotes. Strikingly, the analysis of 43 single-cell genomes shows that Picozoa belong to Archaeplastida, specifically related to red algae and the phagotrophic rhodelphids. These picozoan genomes support the hypothesis that Picozoa lack a plastid, and further reveal no evidence of an early cryptic endosymbiosis with cyanobacteria. These findings change our understanding of plastid evolution as they either represent the first complete plastid loss in a free-living taxon, or indicate that red algae and rhodelphids obtained their plastids independently of other archaeplastids.

Suggested Citation

  • Max E. Schön & Vasily V. Zlatogursky & Rohan P. Singh & Camille Poirier & Susanne Wilken & Varsha Mathur & Jürgen F. H. Strassert & Jarone Pinhassi & Alexandra Z. Worden & Patrick J. Keeling & Thijs J, 2021. "Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26918-0
    DOI: 10.1038/s41467-021-26918-0
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    References listed on IDEAS

    as
    1. Chirag Jain & Luis M. Rodriguez-R & Adam M. Phillippy & Konstantinos T. Konstantinidis & Srinivas Aluru, 2018. "High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    2. Jürgen F. H. Strassert & Iker Irisarri & Tom A. Williams & Fabien Burki, 2021. "A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Jürgen F. H. Strassert & Iker Irisarri & Tom A. Williams & Fabien Burki, 2021. "Author Correction: A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids," Nature Communications, Nature, vol. 12(1), pages 1-2, December.
    4. Gordon Lax & Yana Eglit & Laura Eme & Erin M. Bertrand & Andrew J. Roger & Alastair G. B. Simpson, 2018. "Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes," Nature, Nature, vol. 564(7736), pages 410-414, December.
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