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A robust approach to estimate relative phytoplankton cell abundance from metagenomes

View ORCID ProfileJuan José Pierella Karlusich, View ORCID ProfileEric Pelletier, View ORCID ProfileLucie Zinger, View ORCID ProfileFabien Lombard, View ORCID ProfileAdriana Zingone, View ORCID ProfileSébastien Colin, View ORCID ProfileJosep M. Gasol, View ORCID ProfileRichard G. Dorrell, View ORCID ProfileEleonora Scalco, View ORCID ProfileSilvia G. Acinas, View ORCID ProfilePatrick Wincker, View ORCID ProfileColomban de Vargas, View ORCID ProfileChris Bowler
doi: https://doi.org/10.1101/2021.05.28.446125
Juan José Pierella Karlusich
1Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
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  • ORCID record for Juan José Pierella Karlusich
  • For correspondence: pierella@biologie.ens.fr cbowler@biologie.ens.fr
Eric Pelletier
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
3Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
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Lucie Zinger
1Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
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Fabien Lombard
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
4Sorbonne Universités, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
5Institut Universitaire de France (IUF), Paris, France
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Adriana Zingone
6Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy
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  • ORCID record for Adriana Zingone
Sébastien Colin
7European Molecular Biology Laboratory, Heidelberg, Germany
8Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR 7144, ECOMAP, 29680 Roscoff, France
9Max Planck Institute for Developmental Biology, Tübingen, Germany
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Josep M. Gasol
10Department of Marine Biology and Oceanography, Institut de Ciènces del Mar, CSIC, Barcelona, Spain
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  • ORCID record for Josep M. Gasol
Richard G. Dorrell
1Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
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Eleonora Scalco
6Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy
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Silvia G. Acinas
10Department of Marine Biology and Oceanography, Institut de Ciènces del Mar, CSIC, Barcelona, Spain
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Patrick Wincker
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
3Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
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Colomban de Vargas
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
8Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR 7144, ECOMAP, 29680 Roscoff, France
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Chris Bowler
1Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
2CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France
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  • For correspondence: pierella@biologie.ens.fr cbowler@biologie.ens.fr
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Abstract

Phytoplankton account for >45% of global primary production, and have an enormous impact on aquatic food webs and on the entire Earth System. Their members are found among prokaryotes (cyanobacteria) and multiple eukaryotic lineages containing chloroplasts. Phytoplankton communities are generally studied by PCR amplification of bacterial (16S), nuclear (18S) or chloroplastic (16S) rRNA marker genes from DNA extracted from environmental samples. However, our appreciation of phytoplankton abundance or biomass is limited by PCR-amplification biases, rRNA gene copy number variations across taxa, and the fact that rRNA genes do not provide insights into metabolic traits such as photosynthesis. In addition, rRNA marker genes fail to capture both cyanobacteria and photosynthetic eukaryotes simultaneously. Here, we targeted the photosynthetic gene psbO from metagenomes to circumvent these limitations: the method is PCR-free, and the gene is universally and exclusively present in photosynthetic prokaryotes and eukaryotes, mainly in one copy per genome. We applied and validated this new strategy with the Tara Oceans datasets, and showed improved correlations with flow cytometry and microscopy than when based on rRNA genes. Furthermore, we revealed unexpected features of the ecology of these organisms, such as the high abundance of picocyanobacterial aggregates and symbionts in the ocean, and the decrease in relative abundance of phototrophs towards the larger size classes of marine dinoflagellates. To facilitate the incorporation of psbO in molecular-based surveys, we compiled a curated database of >18,000 unique sequences. Overall, psbO appears to be a promising new gene marker for molecular-based evaluations of entire phytoplankton communities.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.ebi.ac.uk/biostudies/studies/S-BSST659

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 4.0 International license.
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A robust approach to estimate relative phytoplankton cell abundance from metagenomes
Juan José Pierella Karlusich, Eric Pelletier, Lucie Zinger, Fabien Lombard, Adriana Zingone, Sébastien Colin, Josep M. Gasol, Richard G. Dorrell, Eleonora Scalco, Silvia G. Acinas, Patrick Wincker, Colomban de Vargas, Chris Bowler
bioRxiv 2021.05.28.446125; doi: https://doi.org/10.1101/2021.05.28.446125
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A robust approach to estimate relative phytoplankton cell abundance from metagenomes
Juan José Pierella Karlusich, Eric Pelletier, Lucie Zinger, Fabien Lombard, Adriana Zingone, Sébastien Colin, Josep M. Gasol, Richard G. Dorrell, Eleonora Scalco, Silvia G. Acinas, Patrick Wincker, Colomban de Vargas, Chris Bowler
bioRxiv 2021.05.28.446125; doi: https://doi.org/10.1101/2021.05.28.446125

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