Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean

Tom O Delmont; Morgan Gaia; Damien D Hinsinger; Paul Frémont; 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:10.1016/j.xgen.2022.100123

Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean

Cell Genom. 2022 Apr 28;2(5):100123. doi: 10.1016/j.xgen.2022.100123. eCollection 2022 May 11.

Authors

Tom O Delmont^{1

2}, Morgan Gaia^{1

2}, Damien D Hinsinger^{1

2}, Paul Frémont^{1

2}, Chiara Vanni³, Antonio Fernandez-Guerra⁴, A Murat Eren⁵, Artem Kourlaiev^{1

2}, Leo d'Agata^{1

2}, Quentin Clayssen^{1

2}, Emilie Villar¹, Karine Labadie^{1

2}, Corinne Cruaud^{1

2}, Julie Poulain^{1

2}, Corinne Da Silva^{1

2}, Marc Wessner^{1

2}, Benjamin Noel^{1

2}, Jean-Marc Aury^{1

2}; Tara Oceans Coordinators; Colomban de Vargas^{2

15}, Chris Bowler^{2

12}, Eric Karsenti^{2

15

13}, Eric Pelletier^{1

2}, Patrick Wincker^{1

2}, Olivier Jaillon^{1

2}

Collaborators

Tara Oceans Coordinators:
Shinichi Sunagawa⁶, Silvia G Acinas⁷, Peer Bork^{8

9

10}, Eric Karsenti^{11

12

13}, Chris Bowler^{11

12}, Christian Sardet^{11

14}, Lars Stemmann^{11

14}, Colomban de Vargas^{11

15}, Patrick Wincker^{11

16}, Magali Lescot^{11

17}, Marcel Babin^{11

18}, Gabriel Gorsky^{11

14}, Nigel Grimsley^{11

19

20}, Lionel Guidi^{11

14}, Pascal Hingamp^{11

17}, Olivier Jaillon^{11

16}, Stefanie Kandels^{8

11}, Daniele Iudicone²¹, Hiroyuki Ogata²², Stéphane Pesant^{23

24}, Matthew B Sullivan^{25

26

27}, Fabrice Not¹⁵, Karp-Boss Lee²⁸, Emmanuel Boss²⁸, Guy Cochrane²⁹, Michael Follows³⁰, Nicole Poulton³¹, Jeroen Raes^{32

33

34}, Mike Sieracki³¹, Sabrina Speich^{35

36}

Affiliations

¹ Génomique Métabolique, Genoscope, Institut François-Jacob, CEA, CNRS, Université d'Evry, Université Paris-Saclay, 91057 Evry, France.
² Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara GOSEE, 75016 Paris, France.
³ Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Bremen, Germany.
⁴ Lundbeck Foundation GeoGenetics Centre, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁵ Helmholtz Institute for Functional Marine Biodiversity at Oldenburg, Germany.
⁶ Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, EtH Zürich, Zürich, Switzerland.
⁷ Department of Marine Biology and Oceanography, Institute of Marine Sciences-CsiC, Barcelona, Spain.
⁸ Structural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germany.
⁹ Max Delbrück Center for Molecular Medicine, Berlin, Germany.
¹⁰ Department of Bioinformatics, Biocenter, University of Würzburg, Würzburg, Germany.
¹¹ Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara GOsee, Paris, France.
¹² Institut de Biologie de l'ENS, Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France.
¹³ Directors' Research, European Molecular Biology Laboratory, Heidelberg, Germany.
¹⁴ Sorbonne Université, CNRS, Laboratoire D'Océanographie de Villefranche, Villefranche- sur- Mer, France.
¹⁵ Sorbonne Université and CNRS, UMR 7144 (AD2M), ECOMAP, Station Biologique de Roscoff, Roscoff, France.
¹⁶ Génomique Métabolique, Genoscope, Institut de Biologie Francois Jacob, Commissariat à l'Énergie Atomique, CNrs, Université Evry, Université Paris- Saclay, Evry, France.
¹⁷ Aix Marseille Universit/e, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France.
¹⁸ Département de Biologie, Québec Océan and Takuvik Joint International Laboratory (UMI 3376), Université Laval (Canada)-CNRS (France), Université Laval, Quebec, QC, Canada.
¹⁹ CNRS UMR 7232, Biologie Intégrative des Organismes Marins, Banyuls- sur- Mer, France.
²⁰ Sorbonne Universités Paris 06, OOB UPMC, Banyuls- sur- Mer, France.
²¹ Stazione Zoologica Anton Dohrn, Naples, Italy.
²² Institute for Chemical Research, Kyoto University, Kyoto, Japan.
²³ PaNGaea, University of Bremen, Bremen, Germany.
²⁴ MaruM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.
²⁵ Department of Microbiology, The Ohio State University, Columbus, OH, USA.
²⁶ Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH, USA.
²⁷ Center for RNA Biology, The Ohio State University, Columbus, OH, USA.
²⁸ School of Marine Sciences, University of Maine, Orono, ME, USA.
²⁹ European Molecular Biology Laboratory, European Bioinformatics Institute, Welcome Trust Genome Campus, Hinxton, Cambridge, UK.
³⁰ Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.
³¹ Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA.
³² Department of Microbiology and Immunology, Rega Institute, KU Leuven, Leuven, Belgium.
³³ Center for the Biology of Disease, VIB KU Leuven, Leuven, Belgium.
³⁴ Department of Applied Biological Sciences, Vrije Universiteit Brussel, Brussels, Belgium.
³⁵ Department of Geosciences, Laboratoire de Météorologie Dynamique, École Normale Supérieure, Paris, France.
³⁶ Ocean Physics Laboratory, University of Western Brittany, Brest, France.

Abstract

Marine planktonic eukaryotes play critical roles 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, to our knowledge, 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 completely explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years.

Keywords: Planktonic eukaryotes; Tara Oceans; anvi’o; ecology; evolution; functions; genomics; metagenomics.