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Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods

Author

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  • Juan José Pierella Karlusich

    (Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL
    CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE)

  • Eric Pelletier

    (CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay)

  • Fabien Lombard

    (CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    Sorbonne Universités, CNRS, Laboratoire d’Océanographie de Villefranche (LOV)
    Institut Universitaire de France (IUF))

  • Madeline Carsique

    (Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL)

  • Etienne Dvorak

    (Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL)

  • Sébastien Colin

    (European Molecular Biology Laboratory
    Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR 7144, ECOMAP
    Max Planck Institute for Developmental Biology)

  • Marc Picheral

    (CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    Sorbonne Universités, CNRS, Laboratoire d’Océanographie de Villefranche (LOV))

  • Francisco M. Cornejo-Castillo

    (Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR 7144, ECOMAP)

  • Silvia G. Acinas

    (Department of Marine Biology and Oceanography, Institut de Ciènces del Mar, CSIC)

  • Rainer Pepperkok

    (CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    European Molecular Biology Laboratory)

  • Eric Karsenti

    (Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL
    CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    European Molecular Biology Laboratory)

  • Colomban de Vargas

    (CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR 7144, ECOMAP)

  • Patrick Wincker

    (CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
    Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay)

  • Chris Bowler

    (Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL
    CNRS Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE)

  • Rachel A. Foster

    (Stockholm University)

Abstract

Nitrogen fixation has a critical role in marine primary production, yet our understanding of marine nitrogen-fixers (diazotrophs) is hindered by limited observations. Here, we report a quantitative image analysis pipeline combined with mapping of molecular markers for mining >2,000,000 images and >1300 metagenomes from surface, deep chlorophyll maximum and mesopelagic seawater samples across 6 size fractions ( 20 µm). Using imaging and molecular data, we estimate that polyploidy can substantially affect gene abundances of symbiotic versus colony-forming diazotrophs. Our results support the canonical view that larger diazotrophs (>10 μm) dominate the tropical belts, while unicellular cyanobacterial and non-cyanobacterial diazotrophs are globally distributed in surface and mesopelagic layers. We describe co-occurring diazotrophic lineages of different lifestyles and identify high-density regions of diazotrophs in the global ocean. Overall, we provide an update of marine diazotroph biogeographical diversity and present a new bioimaging-bioinformatic workflow.

Suggested Citation

  • Juan José Pierella Karlusich & Eric Pelletier & Fabien Lombard & Madeline Carsique & Etienne Dvorak & Sébastien Colin & Marc Picheral & Francisco M. Cornejo-Castillo & Silvia G. Acinas & Rainer Pepper, 2021. "Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24299-y
    DOI: 10.1038/s41467-021-24299-y
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    Cited by:

    1. Christopher R. Schvarcz & Samuel T. Wilson & Mathieu Caffin & Rosalina Stancheva & Qian Li & Kendra A. Turk-Kubo & Angelicque E. White & David M. Karl & Jonathan P. Zehr & Grieg F. Steward, 2022. "Overlooked and widespread pennate diatom-diazotroph symbioses in the sea," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Katie J. Harding & Kendra A. Turk-Kubo & Esther Wing Kwan Mak & Peter K. Weber & Xavier Mayali & Jonathan P. Zehr, 2022. "Cell-specific measurements show nitrogen fixation by particle-attached putative non-cyanobacterial diazotrophs in the North Pacific Subtropical Gyre," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Benedikt Ehrenfels & Kathrin B. L. Baumann & Robert Niederdorfer & Athanasio S. Mbonde & Ismael A. Kimirei & Thomas Kuhn & Paul M. Magyar & Daniel Odermatt & Carsten J. Schubert & Helmut Bürgmann & Mo, 2023. "Hydrodynamic regimes modulate nitrogen fixation and the mode of diazotrophy in Lake Tanganyika," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Xiyang Dong & Chuwen Zhang & Yongyi Peng & Hong-Xi Zhang & Ling-Dong Shi & Guangshan Wei & Casey R. J. Hubert & Yong Wang & Chris Greening, 2022. "Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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