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Functional repertoire convergence of distantly related eukaryotic plankton lineages revealed by genome-resolved metagenomics

Tom O. Delmont, Morgan Gaia, Damien D. Hinsinger, Paul Fremont, Chiara Vanni, Antonio Fernandez Guerra, A. Murat Eren, Artem Kourlaiev, Leo d’Agata, Quentin Clayssen, Emilie Villar, Karine Labadie, Corinne Cruaud, Julie Poulain, Corinne Da Silva, Marc Wessner, Benjamin Noel, Jean-Marc Aury, Tara Oceans Coordinators, Colomban de Vargas, Chris Bowler, Eric Karsenti, Eric Pelletier, Patrick Wincker, Olivier Jaillon
doi: https://doi.org/10.1101/2020.10.15.341214
Tom O. Delmont
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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  • For correspondence: Tom.Delmont@genoscope.fr
Morgan Gaia
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Damien D. Hinsinger
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Paul Fremont
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Chiara Vanni
3Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359, Bremen, Germany
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Antonio Fernandez Guerra
3Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359, Bremen, Germany
4Lundbeck GeoGenetics Centre, The Globe Institute, University of Copenhagen, 1350 Copenhagen, Denmark
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A. Murat Eren
5Department of Medicine, University of Chicago, Chicago, Illinois 60637, USA
6Bay Paul Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA
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Artem Kourlaiev
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Leo d’Agata
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Quentin Clayssen
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Emilie Villar
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
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Karine Labadie
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Corinne Cruaud
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Julie Poulain
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Corinne Da Silva
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Marc Wessner
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Benjamin Noel
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Jean-Marc Aury
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Colomban de Vargas
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
7Sorbonne Université and CNRS, UMR 7144 (AD2M), ECOMAP, station Biologique de Roscoff, Roscoff, France
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Chris Bowler
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
8Institut de Biologie de l’ENS, Département de Biologie, École Normale supérieure, CNRS, INSERM, Université PSL, Paris, France
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Eric Karsenti
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
7Sorbonne Université and CNRS, UMR 7144 (AD2M), ECOMAP, station Biologique de Roscoff, Roscoff, France
9Directors’ research, European Molecular Biology Laboratory, Heidelberg, Germany
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Eric Pelletier
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Patrick Wincker
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Olivier Jaillon
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Abstract

Marine planktonic eukaryotes play a critical role in global biogeochemical cycles and climate. However, their poor representation in culture collections limits our understanding of the evolutionary history and genomic underpinnings of planktonic ecosystems. Here, we used 280 billion Tara Oceans metagenomic reads from polar, temperate, and tropical sunlit oceans to reconstruct and manually curate more than 700 abundant and widespread eukaryotic environmental genomes ranging from 10 Mbp to 1.3 Gbp. This genomic resource covers a wide range of poorly characterized eukaryotic lineages that complement long-standing contributions from culture collections while better representing plankton in the upper layer of the oceans. We performed the first comprehensive genome-wide functional classification of abundant unicellular eukaryotic plankton, revealing four major groups connecting distantly related lineages. Neither trophic modes of plankton nor its vertical evolutionary history could explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years.

Cover Navigating on the map of plankton genomics with Tara Oceans and anvi’o: a comprehensive genome-resolved metagenomic survey dedicated to eukaryotic plankton.

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Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The functional repertoire classification of unicellular eukaryotes is now performed in both the known and unknown coding space. This additional analysis. This allowed us to identify a functional repertoire convergence of distantly related eukaryotic plankton lineages in both the known and unknown coding sequence space, the latter representing a substantial amount of biologically relevant gene diversity.

  • https://www.genoscope.cns.fr/tara/

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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 4.0 International license.
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Posted January 23, 2021.
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Functional repertoire convergence of distantly related eukaryotic plankton lineages revealed by genome-resolved metagenomics
Tom O. Delmont, Morgan Gaia, Damien D. Hinsinger, Paul Fremont, Chiara Vanni, Antonio Fernandez Guerra, A. Murat Eren, Artem Kourlaiev, Leo d’Agata, Quentin Clayssen, Emilie Villar, Karine Labadie, Corinne Cruaud, Julie Poulain, Corinne Da Silva, Marc Wessner, Benjamin Noel, Jean-Marc Aury, Tara Oceans Coordinators, Colomban de Vargas, Chris Bowler, Eric Karsenti, Eric Pelletier, Patrick Wincker, Olivier Jaillon
bioRxiv 2020.10.15.341214; doi: https://doi.org/10.1101/2020.10.15.341214
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Functional repertoire convergence of distantly related eukaryotic plankton lineages revealed by genome-resolved metagenomics
Tom O. Delmont, Morgan Gaia, Damien D. Hinsinger, Paul Fremont, Chiara Vanni, Antonio Fernandez Guerra, A. Murat Eren, Artem Kourlaiev, Leo d’Agata, Quentin Clayssen, Emilie Villar, Karine Labadie, Corinne Cruaud, Julie Poulain, Corinne Da Silva, Marc Wessner, Benjamin Noel, Jean-Marc Aury, Tara Oceans Coordinators, Colomban de Vargas, Chris Bowler, Eric Karsenti, Eric Pelletier, Patrick Wincker, Olivier Jaillon
bioRxiv 2020.10.15.341214; doi: https://doi.org/10.1101/2020.10.15.341214

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