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

Type Article
Date 2019-03
Language English
Author(s) Caputi LuigiORCID1, Carradec QuentinORCID2, 3, 4, 5, Eveillard Damien5, 6, Kirilovsky Amos7, 8, Pelletier Eric2, 3, 4, 5, Karlusich Juan J. Pierella5, 7, Vieira Fabio Rocha Jimenez5, 7, Villar Emilie7, 9, Chaffron SamuelORCID7, 8, Malviya Shruti7, 10, Scalco Eleonora1, Acinas Silvia G.11, Alberti Adriana2, 5, Aury Jean-Marc2, Benoiston Anne-Sophie7, 12, Bertrand Arnaud2, Biard Tristan9, Bittner Lucie7, 9, 12, Boccara Martine7, Brum Jennifer R.13, 14, Brunet Cedric1, Busseni Greta1, Carratala Anna15, Claustre Herve16, Coelho Luis Pedro17, Colin Sbastien5, 7, 9, D'Aniello Salvatore1, Da Silva Corinne3, 5, Del Core Marianna18, Dore Hugo9, Gasparini Stephane16, Kokoszka Florian1, 7, 19, Jamet Jean-Louis20, Lejeusne Christophe1, 21, Lepoivre Cyrille22, Lescot Magali5, 23, Lima-Mendez Gipsi24, 25, Lombard FabienORCID5, 16, Lukes Julius26, 27, Maillet Nicolas1, 28, Madoui Mohammed-Amin2, 3, 4, Martinez ElodieORCID29, Mazzocchi Maria Grazia1, Neou Mario B.2, 3, 4, Paz-Yepes Javier8, Poulain Julie2, 5, Ramondenc Simon16, Romagnan Jean-Baptiste30, Roux Simon14, Manta Daniela Salvagio18, Sanges Remo1, Speich Sabrina5, 19, Sprovieri Mario18, Sunagawa ShinichiORCID17, Taillandier Vincent16, Tanaka Atsuko7, Tirichine Leila7, Trottier Camille6, Uitz Julia16, Veluchamy Alaguraj7, Vesela Jana26, Vincent Flora7, Yau ShereeORCID, Kandels-Lewis Stefanie17, Searson Sarah16, Dimier Cline7, 9, Picheral Marc5, 16, Bork Peer17, Boss EmmanuelORCID, de Vargas Colomban5, 9, Follows Michael J., Grimsley Nigel5, Guidi LionelORCID5, 16, Hingamp Pascal5, 23, Karsenti Eric5, 7, Sordino Paolo1, Stemmann Lars5, 16, Sullivan Matthew B.14, Tagliabue Alessandro, Zingone Adriana1, Garczarek Laurence9, D'Ortenzio Fabrizio16, Testor Pierre, Not Fabrice9, D'Alcala Maurizio Ribera1, Wincker Patrick2, 3, 4, 5, Bowler Chris5, 7, Iudicone Daniele1, Gorsky Gabriel16, Jaillon Olivier2, 3, Karp-Boss Lee38, Krzic Uros44, Ogata Hiroyuki45, Pesant Stephane46, 47, Raes Jeroen24, Reynaud Emmanuel G.48, Sardet Christian16, Sieracki Mike49, 50, Velayoudon Didier51, Weissenbach Jean2, 3, 4
Affiliation(s) 1 : Stn Zool Anton Dohrn, Naples, Italy.
2 : CEA, Genoscope, Inst Francois Jacob, Evry, France.
3 : CNRS UMR, Evry, France.
4 : Univ Paris Saclay, Univ Evry Val dEssonne, Evry, France.
5 : Res Federat Study Global Ocean Syst Ecol & Evolut, FR2022 GOSEE, Paris, France.
6 : Univ Nantes, LS2N, IMT Atlantique, Ecole Cent Nantes,CNRS, Nantes, France.
7 : PSL Univ Paris, Inst Biol, INSERM, CNRS,Ecole Normale Super IBENS,Ecole Normale Supe, Paris, France.
8 : Ctr Rech Cordeliers, Lab Integrat Canc Immunol, UMRS1138, INSERM, Paris, France.
9 : UPMC Univ Paris 06, Stn Biol Roscoff, CNRS, Sorbonne Univ,UMR 7144, Pl Georges Teissier, Roscoff, France.
10 : Tata Inst Fundamental Res, Natl Ctr Biol Sci, Simons Ctr Study Living Machines, Bangalore, Karnataka, India.
11 : CSIC, Dept Marine Biol & Oceanog, Inst Marine Sci ICM, Barcelona, Spain.
12 : Univ Antilles, Sorbonne Univ, Inst Systemat Evolut Biodiversite ISYEB, Museum Natl Hist Nat,CNRS,EPHE, Paris, France.
13 : Louisiana State Univ, Dept Oceanog & Coastal Sci, Baton Rouge, LA 70803 USA.
14 : Ohio State Univ, Dept Microbiol & Civil Environm & Geodet Engn, Columbus, OH 43210 USA.
15 : Ecole Polytech Fed Lausanne, Lab Environm Chem, Sch Architecture Civil & Environm Engn ENAC, Lausanne, Switzerland.
16 : Sorbonne Univ, Inst Mer Villefranche Sur Mer, Lab Oceanog Villefranche, CNRS,UMR 7093, Villefranche Sur Mer, France.
17 : European Mol Biol Lab, Struct & Computat Biol Unit, Heidelberg, Germany.
18 : Inst Anthrop Impacts & Sustainabil Marine Environ, Capo Granitola, Torretta Granit, Italy.
19 : PSL Res Univ, LMD Lab Meteorol Dynam, Ecole Normale Super Paris, Paris, France.
20 : Univ Toulon & Var, Aix Marseille Univ, CNRS INSU, IRD,MIO UM 110 Mediterranean Inst Oceanog, La Garde, France.
21 : Avignon Univ, Aix Marseille Univ, Inst Mediterraneen Biodiversite & Ecol Marine & C, Stn Marine Endoume,UMR 7263 CNRS,IRD, Marseille, France.
22 : Aix Marseille Univ, Inst Microbiol Mediterranee FR3479, CNRS, Informat Genom & Struct,UMR7256, ParcSci Luminy, Marseille, France.
23 : Univ Toulon & Var, Aix Marseille Univ, MIO, CNRS,IRD, Marseille, France.
24 : Katholieke Univ Leuven, Dept Microbiol & Immunol, Rega Inst, Leuven, Belgium.
25 : VIB, Ctr Biol Dis, Leuven, Belgium.
26 : Biol Ctr CAS, Inst Parasitol, Ceske Budejovice, Czech Republic.
27 : Univ South Bohemia, Fac Sci, Ceske Budejovice, Czech Republic.
28 : Inst Pasteur, USR 3756 IP CNRS, Bioinformat & Biostat Hub, C3BI, Paris, France.
29 : Univ Brest, Ifremer, IUEM, CNRS,LOPS,IRD, Brest, France.
30 : IFREMER, Physiol & Biotechnol Algae Lab, Rue IledYeu, Nantes, France.
31 : Inst Microbiol, Dept Biol, Zurich, Switzerland.
32 : Univ Nantes, Fac Sci & Tech, URI, CNRS UMR6286, Nantes, France.
33 : King Abdullah Univ Sci & Technol, Biol & Environm Sci & Engn Div, Thuwal, Saudi Arabia.
34 : UPMC Univ Paris 06, Observ Oceanol, BIOM, CNRS,UMR 7232,Sorbonne Univ, Banyuls Sur Mer, France.
35 : Directors Res European Mol Biol Lab, Meyerhofstr 1, Heidelberg, Germany.
36 : Max Delbruck Ctr Mol Med, Berlin, Germany.
37 : Univ Wurzburg, Bioctr, Dept Bioinformat, Wurzburg, Germany.
38 : Univ Maine, Sch Marine Sci, Orono, ME USA.
39 : Sorbonne Univ, ECOMAP, UMR7144, Stn Biol Roscoff,CNRS, Roscoff, France.
40 : MIT, Dept Earth Atmospher & Planetary Sci, Cambridge, MA USA.
41 : Univ Hawaii, Dept Oceanog, Honolulu, HI 96822 USA.
42 : Univ Liverpool, Sch Environm Sci, Dept Earth Ocean & Ecol Sci, Liverpool, Merseyside, England.
43 : Univ Paris 06, Sorbonne Univ, Lab LOCEAN, UPMC,CNRS,IRD,MNHN, Paris, France.
44 : European Mol Biol Lab, Cell Biol & Biophys, Heidelberg, Germany.
45 : Kyoto Univ, Inst Chem Res, Uji, Kyoto, Japan.
46 : Univ Bremen, Ctr Marine Environm Sci, MARUM, Bremen, Germany.
47 : Univ Bremen, Data Publisher Earth & Environm Sci, PANGAEA, Bremen, Germany.
48 : Univ Coll Dublin, Earth Inst, Dublin, Ireland.
49 : Natl Sci Fdn, 4201 Wilson Blvd, Arlington, VA 22230 USA.
50 : Bigelow Lab Ocean Sci East Boothbay, Boothbay, ME USA.
51 : DVIP Consulting, Sevres, France.
Source Global Biogeochemical Cycles (0886-6236) (American Geophysical Union (AGU)), 2019-03 , Vol. 33 , N. 3 , P. 391-419
DOI 10.1029/2018GB006022
WOS© Times Cited 30
Abstract

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. Publisher's official version : https://doi.org/10.1029/2018GB006022 , Open Access version : https://archimer.ifremer.fr/doc/00475/58680/