Community-Level Responses to Iron Availability in Open Ocean Planktonic Ecosystems

Predicting responses of plankton to variations in essential nutrients is hampered by limited in situ measurements, a poor understanding of community composition, and the lack of reference gene catalogs for key taxa. Iron is a key driver of plankton dynamics and, therefore, of global biogeochemical cycles and climate. To assess the impact of iron availability on plankton communities we explored the comprehensive bio‐oceanographic and ‐omics datasets from Tara Oceans in the context of the iron products from two state‐of‐the‐art global scale biogeochemical models. We obtained novel information about adaptation and acclimation towards iron in a range of phytoplankton, including picocyanobacteria and diatoms, and identified whole sub‐communities co‐varying with iron. Many of the observed global patterns were recapitulated in the Marquesas archipelago, where frequent plankton blooms are believed to be caused by natural iron fertilization, although they are not captured in large scale biogeochemical models. This work provides a proof‐of‐concept that integrative analyses, spanning from genes to ecosystems and viruses to zooplankton, can disentangle the complexity of plankton communities and can lead to more accurate formulations of resource bioavailability in biogeochemical models, thus improving our understanding of plankton resilience in a changing environment.

Plain Language Summary

Marine phytoplankton require iron for their growth and proliferation. According to John Martin's iron hypothesis, fertilizing the ocean with iron could dramatically increase photosynthetic activity, thus representing a biological means to counteract global warming. However, while there is a constantly growing knowledge of how iron is distributed in the ocean and about its role in cellular processes in marine photosynthetic groups such as diatoms and cyanobacteria, less is known about how iron availability shapes plankton communities and how they respond to it. In the present work, we exploited recently published Tara Oceans datasets to address these questions. We firstly defined specific subcommunities of co‐occurring organisms that are directly related to iron availability in the oceans. We then identified specific patterns of adaptation and acclimation to iron in different groups of phytoplankton. Finally, we validated our global results at local scale, specifically in the Marquesas archipelago, where recurrent iron‐driven phytoplankton blooms are believed to be a result of iron fertilization. By integrating global data with a localized response we provide a framework for understanding the resilience of plankton ecosystems in a changing environment.

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Caputi Luigi, Carradec Quentin, Eveillard Damien, Kirilovsky Amos, Pelletier Eric, Karlusich Juan J. Pierella, Vieira Fabio Rocha Jimenez, Villar Emilie, Chaffron Samuel, Malviya Shruti, Scalco Eleonora, Acinas Silvia G., Alberti Adriana, Aury Jean-Marc, Benoiston Anne-Sophie, Bertrand Arnaud, Biard Tristan, Bittner Lucie, Boccara Martine, Brum Jennifer R., Brunet Cedric, Busseni Greta, Carratala Anna, Claustre Herve, Coelho Luis Pedro, Colin Sbastien, D'Aniello Salvatore, Da Silva Corinne, Del Core Marianna, Dore Hugo, Gasparini Stephane, Kokoszka Florian, Jamet Jean-Louis, Lejeusne Christophe, Lepoivre Cyrille, Lescot Magali, Lima-Mendez Gipsi, Lombard Fabien, Lukes Julius, Maillet Nicolas, Madoui Mohammed-Amin, Martinez Elodie, Mazzocchi Maria Grazia, Neou Mario B., Paz-Yepes Javier, Poulain Julie, Ramondenc Simon, Romagnan Jean-Baptiste, Roux Simon, Manta Daniela Salvagio, Sanges Remo, Speich Sabrina, Sprovieri Mario, Sunagawa Shinichi, Taillandier Vincent, Tanaka Atsuko, Tirichine Leila, Trottier Camille, Uitz Julia, Veluchamy Alaguraj, Vesela Jana, Vincent Flora, Yau Sheree, Kandels-Lewis Stefanie, Searson Sarah, Dimier Cline, Picheral Marc, Bork Peer, Boss Emmanuel, de Vargas Colomban, Follows Michael J., Grimsley Nigel, Guidi Lionel, Hingamp Pascal, Karsenti Eric, Sordino Paolo, Stemmann Lars, Sullivan Matthew B., Tagliabue Alessandro, Zingone Adriana, Garczarek Laurence, D'Ortenzio Fabrizio, Testor Pierre, Not Fabrice, D'Alcala Maurizio Ribera, Wincker Patrick, Bowler Chris, Iudicone Daniele, Gorsky Gabriel, Jaillon Olivier, Karp-Boss Lee, Krzic Uros, Ogata Hiroyuki, Pesant Stephane, Raes Jeroen, Reynaud Emmanuel G., Sardet Christian, Sieracki Mike, Velayoudon Didier, Weissenbach Jean (2019). Community-Level Responses to Iron Availability in Open Ocean Planktonic Ecosystems. Global Biogeochemical Cycles. 33 (3). 391-419. https://doi.org/10.1029/2018GB006022, https://archimer.ifremer.fr/doc/00475/58680/

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