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

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 pic...

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Main Authors: 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 Muratore, Rogelio A. Rodriguez-Gonzalez, Shengyun Peng, Kevin W. Becker, Daniel R. Mende, E. Virginia Armbrust, David A. Caron, Debbie Lindell, Angelicque E. White, François Ribalet, Joshua S. Weitz
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-46165-3
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author 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 Muratore
Rogelio A. Rodriguez-Gonzalez
Shengyun Peng
Kevin W. Becker
Daniel R. Mende
E. Virginia Armbrust
David A. Caron
Debbie Lindell
Angelicque E. White
François Ribalet
Joshua S. Weitz
author_facet 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 Muratore
Rogelio A. Rodriguez-Gonzalez
Shengyun Peng
Kevin W. Becker
Daniel R. Mende
E. Virginia Armbrust
David A. Caron
Debbie Lindell
Angelicque E. White
François Ribalet
Joshua S. Weitz
author_sort Stephen J. Beckett
collection DOAJ
description 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.
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spelling doaj.art-846c121df20d4f70babafe4c8356cd152024-03-10T12:17:45ZengNature PortfolioNature Communications2041-17232024-03-0115111310.1038/s41467-024-46165-3Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical GyreStephen J. Beckett0David Demory1Ashley R. Coenen2John R. Casey3Mathilde Dugenne4Christopher L. Follett5Paige Connell6Michael C. G. Carlson7Sarah K. Hu8Samuel T. Wilson9Daniel Muratore10Rogelio A. Rodriguez-Gonzalez11Shengyun Peng12Kevin W. Becker13Daniel R. Mende14E. Virginia Armbrust15David A. Caron16Debbie Lindell17Angelicque E. White18François Ribalet19Joshua S. Weitz20School of Biological Sciences, Georgia Institute of TechnologySchool of Biological Sciences, Georgia Institute of TechnologySchool of Physics, Georgia Institute of TechnologyDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i at MānoaDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i at MānoaDepartment of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of TechnologyDepartment of Biological Sciences, University of Southern CaliforniaFaculty of Biology, Technion – Israel Institute of TechnologyDepartment of Biological Sciences, University of Southern CaliforniaDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i at MānoaSchool of Biological Sciences, Georgia Institute of TechnologySchool of Biological Sciences, Georgia Institute of TechnologySchool of Biological Sciences, Georgia Institute of TechnologyDepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic InstitutionDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i at MānoaSchool of Oceanography, University of WashingtonDepartment of Biological Sciences, University of Southern CaliforniaFaculty of Biology, Technion – Israel Institute of TechnologyDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i at MānoaSchool of Oceanography, University of WashingtonSchool of Biological Sciences, Georgia Institute of TechnologyAbstract 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.https://doi.org/10.1038/s41467-024-46165-3
spellingShingle 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 Muratore
Rogelio A. Rodriguez-Gonzalez
Shengyun Peng
Kevin W. Becker
Daniel R. Mende
E. Virginia Armbrust
David A. Caron
Debbie Lindell
Angelicque E. White
François Ribalet
Joshua S. Weitz
Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre
Nature Communications
title Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre
title_full Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre
title_fullStr Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre
title_full_unstemmed Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre
title_short Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre
title_sort disentangling top down drivers of mortality underlying diel population dynamics of prochlorococcus in the north pacific subtropical gyre
url https://doi.org/10.1038/s41467-024-46165-3
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