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Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre

Author

Listed:
  • Stephen J. Beckett

    (Georgia Institute of Technology
    University of Maryland)

  • David Demory

    (Georgia Institute of Technology
    Laboratoire de Biodiversité et Biotechnologies Microbiennes (LBBM), Observatoire Océanologique)

  • Ashley R. Coenen

    (Georgia Institute of Technology)

  • John R. Casey

    (University of Hawai’i at Mānoa
    University of Hawai’i at Mānoa
    Massachusetts Institute of Technology
    Lawrence Livermore National Laboratory)

  • Mathilde Dugenne

    (University of Hawai’i at Mānoa
    University of Hawai’i at Mānoa
    Laboratoire d’Océanographie de Villefranche-sur-Mer (LOV))

  • Christopher L. Follett

    (Massachusetts Institute of Technology
    University of Liverpool)

  • Paige Connell

    (University of Southern California
    Biology Department, San Diego Mesa College)

  • Michael C. G. Carlson

    (Technion – Israel Institute of Technology
    California State University)

  • Sarah K. Hu

    (University of Southern California
    Woods Hole Oceanographic Institution
    Texas A&M University)

  • Samuel T. Wilson

    (University of Hawai’i at Mānoa
    University of Hawai’i at Mānoa
    Newcastle University)

  • Daniel Muratore

    (Georgia Institute of Technology
    Santa Fe Institute)

  • Rogelio A. Rodriguez-Gonzalez

    (Georgia Institute of Technology)

  • Shengyun Peng

    (Georgia Institute of Technology
    Adobe)

  • Kevin W. Becker

    (Woods Hole Oceanographic Institution
    GEOMAR Helmholtz Centre for Ocean Research)

  • Daniel R. Mende

    (University of Hawai’i at Mānoa
    University of Hawai’i at Mānoa
    Department of Medical Microbiology, Academic Medical Centre, University of Amsterdam)

  • E. Virginia Armbrust

    (University of Washington)

  • David A. Caron

    (University of Southern California)

  • Debbie Lindell

    (Technion – Israel Institute of Technology)

  • Angelicque E. White

    (University of Hawai’i at Mānoa
    University of Hawai’i at Mānoa)

  • François Ribalet

    (University of Washington)

  • Joshua S. Weitz

    (Georgia Institute of Technology
    University of Maryland
    Georgia Institute of Technology
    École Normale Supérieure)

Abstract

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers in this environment function as the predominant top-down factor despite high standing viral particle densities. The model-data fits also reveal the ecological relevance of light-dependent viral traits and non-canonical factors to cellular loss. Finally, we leverage sensitivity analyses to demonstrate how variation in life history traits across distinct oceanic contexts, including variation in viral adsorption and grazer clearance rates, can transform the quantitative and even qualitative importance of top-down controls in shaping Prochlorococcus population dynamics.

Suggested Citation

  • Stephen J. Beckett & David Demory & Ashley R. Coenen & John R. Casey & Mathilde Dugenne & Christopher L. Follett & Paige Connell & Michael C. G. Carlson & Sarah K. Hu & Samuel T. Wilson & Daniel Murat, 2024. "Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46165-3
    DOI: 10.1038/s41467-024-46165-3
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    References listed on IDEAS

    as
    1. Kevin W. Becker & James R. Collins & Bryndan P. Durham & Ryan D. Groussman & Angelicque E. White & Helen F. Fredricks & Justin E. Ossolinski & Daniel J. Repeta & Paul Carini & E. Virginia Armbrust & B, 2018. "Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    2. Stephen J Beckett & Joshua S Weitz, 2017. "Disentangling niche competition from grazing mortality in phytoplankton dilution experiments," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-12, May.
    3. Jed A. Fuhrman, 1999. "Marine viruses and their biogeochemical and ecological effects," Nature, Nature, vol. 399(6736), pages 541-548, June.
    4. Ryan N Gutenkunst & Joshua J Waterfall & Fergal P Casey & Kevin S Brown & Christopher R Myers & James P Sethna, 2007. "Universally Sloppy Parameter Sensitivities in Systems Biology Models," PLOS Computational Biology, Public Library of Science, vol. 3(10), pages 1-8, October.
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