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

• Published in: Nature communications Vol. 15; no. 1; p. 2105
• Main Authors: Beckett, Stephen J., Demory, David, Coenen, Ashley R., Casey, John R., Dugenne, Mathilde, Follett, Christopher L., Connell, Paige, Carlson, Michael C. G., Hu, Sarah K., Wilson, Samuel T., Muratore, Daniel, Rodriguez-Gonzalez, Rogelio A., Peng, Shengyun, Becker, Kevin W., Mende, Daniel R., Armbrust, E. Virginia, Caron, David A., Lindell, Debbie, White, Angelicque E., Ribalet, François, Weitz, Joshua S.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 07.03.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/158/1144; 631/158/2446/2447; 631/326/171/1878; Bacteriology; Biodiversity and Ecology; Data integration; Earth Sciences; ENVIRONMENTAL SCIENCES; Estimates; Food chains; Food webs; Humanities and Social Sciences; Infections; Life history; Life Sciences; Marine ecosystems; Microbiology and Parasitology; Mortality; multidisciplinary; Oceanography; Oscillations; Photosynthesis; Plankton; Population dynamics; Population studies; Populations; Primary production; Prochlorococcus; Science; Science (multidisciplinary); Sciences of the Universe; Sensitivity analysis; Surface water; Time series; Viral infections
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-46165-3

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. This study shows that a multitrophic community model jointly recapitulates diel rhythms in abundances of Prochlorococcus picocyanobacteria, as well as viral infection, viral abundances and grazer abundances. Model-data integration implies that grazing predominantly controls Prochlorococcus abundances in surface waters of the North Pacific Subtropical Gyre, despite high viral densities.