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Picozoa are archaeplastids without plastid

View ORCID ProfileMax E. Schön, View ORCID ProfileVasily V. Zlatogursky, Rohan P. Singh, Camille Poirier, View ORCID ProfileSusanne Wilken, View ORCID ProfileVarsha Mathur, View ORCID ProfileJürgen F. H. Strassert, View ORCID ProfileJarone Pinhassi, View ORCID ProfileAlexandra Z. Worden, View ORCID ProfilePatrick J. Keeling, View ORCID ProfileThijs J. G. Ettema, View ORCID ProfileJeremy G. Wideman, View ORCID ProfileFabien Burki
doi: https://doi.org/10.1101/2021.04.14.439778
Max E. Schön
1Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden
2Department of Cell and Molecular Biology, Program in Molecular Evolution, Uppsala University, Uppsala, Sweden
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Vasily V. Zlatogursky
1Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden
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Rohan P. Singh
3Biodesign Center for Mechanisms of Evolution, School of Life Sciences, Arizona State University, Tempe, AZ, USA
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Camille Poirier
4Ocean EcoSystems Biology, RD3, GEOMAR Helmholtz Centre for Ocean Research Kiel, Germany
5Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA
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Susanne Wilken
5Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA
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Varsha Mathur
6Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada
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Jürgen F. H. Strassert
1Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden
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Jarone Pinhassi
7Centre for Ecology and Evolution in Microbial Model Systems – EEMiS, Linnaeus University, Kalmar, Sweden
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  • ORCID record for Jarone Pinhassi
Alexandra Z. Worden
4Ocean EcoSystems Biology, RD3, GEOMAR Helmholtz Centre for Ocean Research Kiel, Germany
5Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA
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Patrick J. Keeling
6Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada
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Thijs J. G. Ettema
8Laboratory of Microbiology, Wageningen University and Research, NL-6708 WE Wageningen, The Netherlands
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Jeremy G. Wideman
3Biodesign Center for Mechanisms of Evolution, School of Life Sciences, Arizona State University, Tempe, AZ, USA
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Fabien Burki
1Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden
9Science for Life Laboratory, Uppsala University, Uppsala, Sweden
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  • For correspondence: fabien.burki@ebc.uu.se
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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, and are widely assumed to have a single origin. Here, we used 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, we find based on the analysis of 43 single-cell genomes that Picozoa belong to Archaeplastida as a robust sister group to the clade containing red algae and the phagotrophic rhodelphids. Our analyses of this extensive data support the hypothesis that Picozoa lack a plastid, and further show no evidence for an early cryptic endosymbiosis with cyanobacteria. The position of Picozoa in the eukaryotic tree represents the first known case of a plastid-lacking lineage closely related to one of the main archaeplastid branches. The implications of these findings for our understanding of plastid evolution are unprecedented, and can either be interpreted as the first report of complete plastid loss in a free-living taxon, or as an indication that red algae and rhodelphids obtained their plastids independently of other archaeplastids.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://doi.org/10.6084/m9.figshare.c.5388176

  • https://github.com/maxemil/picozoa-scripts

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Picozoa are archaeplastids without plastid
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. G. Ettema, Jeremy G. Wideman, Fabien Burki
bioRxiv 2021.04.14.439778; doi: https://doi.org/10.1101/2021.04.14.439778
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Picozoa are archaeplastids without plastid
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. G. Ettema, Jeremy G. Wideman, Fabien Burki
bioRxiv 2021.04.14.439778; doi: https://doi.org/10.1101/2021.04.14.439778

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