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The biological carbon pump is the process by which CO2 is transformed to organic carbon via photosynthesis, exported through sinking particles, and finally sequestered in the deep ocean. While the intensity of the pump correlates with plankton community composition, the underlying ecosystem structure driving the process remains largely uncharacterized. Here we use environmental and metagenomic data gathered during the Tara Oceans expedition to improve our understanding of carbon export in the oligotrophic ocean. We show that specific plankton communities, from the surface and deep chlorophyll maximum, correlate with carbon export at 150 m and highlight unexpected taxa such as Radiolaria and alveolate parasites, as well as Synechococcus and their phages, as lineages most strongly associated with carbon export in the subtropical, nutrient-depleted, oligotrophic ocean. Additionally, we show that the relative abundance of a few bacterial and viral genes can predict a significant fraction of the variability in carbon export in these regions.

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Change history

  • 12 February 2016

    The author affiliations and corresponding authors were corrected. The Supplementary Material listing the Tara Oceans consortium members was also updated.


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We thank the commitment of the following people and sponsors: CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, Fund for Scientific Research – Flanders, Rega Institute, KU Leuven, The French Ministry of Research, the French Government ‘Investissements d’Avenir’ programmes OCEANOMICS (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX-54), PSL* Research University (ANR-11-IDEX-0001-02), ANR (projects POSEIDON/ANR-09-BLAN-0348, PHYTBACK/ANR-2010-1709-01, PROMETHEUS/ANR-09-PCS-GENM-217, TARA-GIRUS/ANR-09-PCS-GENM-218, SAMOSA, ANR-13-ADAP-0010), European Union FP7 (MicroB3/No.287589, ERC Advanced Grant Award to C.B. (Diatomite: 294823), Gordon and Betty Moore Foundation grant (#3790 and #2631) and the UA Technology and Research Initiative Fund and the Water, Environmental, and Energy Solutions Initiative to M.B.S., the Italian Flagship Program RITMARE to D.I., the Spanish Ministry of Science and Innovation grant CGL2011-26848/BOS MicroOcean PANGENOMICS to S.G.A., TANIT (CONES 2010-0036) from the Agència de Gestió d´Ajusts Universitaris i Reserca to S.G.A., JSPS KAKENHI grant number 26430184 to H.O., and FWO, BIO5, Biosphere 2 to M.B.S. We also thank the support and commitment of Agnès b. and Etienne Bourgois, the Veolia Environment Foundation, Region Bretagne, Lorient Agglomeration, World Courier, Illumina, the EDF Foundation, FRB, the Prince Albert II de Monaco Foundation, the Tara schooner and its captains and crew. We thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expedition. We are also grateful to the French Ministry of Foreign Affairs for supporting the expedition and to the countries who graciously granted sampling permissions. Tara Oceans would not exist without continuous support from 23 institutes ( The authors further declare that all data reported herein are fully and freely available from the date of publication, with no restrictions, and that all of the samples, analyses, publications, and ownership of data are free from legal entanglement or restriction of any sort by the various nations whose waters the Tara Oceans expedition sampled in. This article is contribution number 34 of Tara Oceans.

Author information

Author notes

    • Simon Roux
    • , Léo Berline
    • , Jennifer R. Brum
    • , Shruti Malviya
    •  & Matthew B. Sullivan

    Present addresses: Department of Microbiology, The Ohio State University, Columbus, Ohio 43210, USA (S.R., J.R.B.); Department of Microbiology, and Department of Civil, Environmental and Geodetic Engineering, The Ohio Sate University, Colombus, Ohio 43210, USA (M.B.S.); Aix Marseille Université, CNRS/INSU, Université de Toulon, IRD, Mediterranean Institute of Oceanography (MIO) UM 110, 13288, Marseille, France (L.B.); Biological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, Goa 403 004, India (S.M.).

    • Lionel Guidi
    • , Samuel Chaffron
    • , Lucie Bittner
    •  & Damien Eveillard

    These authors contributed equally to this work.


  1. Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire d’oceanographie de Villefranche (LOV), Observatoire Océanologique, 06230 Villefranche-sur-Mer, France

    • Lionel Guidi
    • , Léo Berline
    • , Marc Picheral
    • , Sarah Searson
    • , Lars Stemmann
    •  & Gabriel Gorsky
  2. Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96822, USA

    • Lionel Guidi
    •  & Sarah Searson
  3. Department of Microbiology and Immunology, Rega Institute, KU Leuven, Herestraat 49, 3000 Leuven, Belgium

    • Samuel Chaffron
    • , Youssef Darzi
    •  & Jeroen Raes
  4. Center for the Biology of Disease, VIB, Herestraat 49, 3000 Leuven, Belgium

    • Samuel Chaffron
    • , Youssef Darzi
    •  & Jeroen Raes
  5. Department of Applied Biological Sciences, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium

    • Samuel Chaffron
    •  & Jeroen Raes
  6. Sorbonne Universités, UPMC Univ Paris 06, CNRS, Institut de Biologie Paris-Seine (IBPS), Evolution Paris Seine, F-75005, Paris, France

    • Lucie Bittner
  7. Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l’Ecole Normale Supérieure (IBENS), CNRS UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France

    • Lucie Bittner
    • , Shruti Malviya
    • , Eric Karsenti
    •  & Chris Bowler
  8. Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29680 Roscoff, France

    • Lucie Bittner
    • , Stephane Audic
    • , Céline Dimier
    • , Fabrice Not
    •  & Colomban de Vargas
  9. LINA UMR 6241, Université de Nantes, EMN, CNRS, 44322 Nantes, France

    • Damien Eveillard
    •  & Abdelhalim Larhlimi
  10. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA

    • Simon Roux
    • , Jennifer R. Brum
    • , Julio Cesar Ignacio Espinoza
    •  & Matthew B. Sullivan
  11. Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany

    • Luis Pedro Coelho
    • , Shinichi Sunagawa
    • , Stefanie Kandels-Lewis
    •  & Peer Bork
  12. Directors’ Research European Molecular Biology Laboratory Meyerhofstr. 1, 69117 Heidelberg, Germany

    • Stefanie Kandels-Lewis
    •  & Eric Karsenti
  13. CEA - Institut de Génomique, GENOSCOPE, 2 rue Gaston Crémieux, 91057 Evry, France

    • Julie Poulain
    • , Jean Weissenbach
    •  & Patrick Wincker
  14. Aix Marseille Université, CNRS, IGS, UMR 7256, 13288 Marseille, France

    • Pascal Hingamp
  15. Department of Geosciences, Laboratoire de Météorologie Dynamique (LMD), Ecole Normale Supérieure, 24 rue Lhomond, 75231 Paris CEDEX 05, France

    • Sabrina Speich
  16. Dept of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA

    • Mick Follows
  17. School of Marine Sciences, University of Maine, Orono, Maine 04469, USA

    • Lee Karp-Boss
    •  & Emmanuel Boss
  18. Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan

    • Hiroyuki Ogata
  19. PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, 28359 Bremen, Germany

    • Stephane Pesant
  20. MARUM, Center for Marine Environmental Sciences, University of Bremen, 28359 Bremen, Germany

    • Stephane Pesant
  21. CNRS, UMR 8030, CP 5706 Evry, France

    • Jean Weissenbach
    •  & Patrick Wincker
  22. Université d’Evry, UMR 8030, CP 5706 Evry, France

    • Jean Weissenbach
    •  & Patrick Wincker
  23. Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM)-CSIC, Pg. Marítim de la Barceloneta 37-49, Barcelona E0800, Spain

    • Silvia G. Acinas
  24. Max-Delbrück-Centre for Molecular Medicine, 13092 Berlin, Germany

    • Peer Bork
  25. Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy

    • Daniele Iudicone


  1. Tara Oceans Consortium Coordinators

    A list of authors and affiliations appears in the Supplementary Information.


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L.G., S.C., Lu.B. and D.E. designed the study and wrote the paper. C.D., M.P., J.P. and Sa.S. collected Tara Oceans samples. S.K.-L. managed the logistics of the Tara Oceans project. L.G. and M.P. analysed oceanographic data. S.C. and Lu.B. analysed taxonomic data. S.C., Lu.B., D.E. and S.R. performed the genomic and statistical analyses. A.L., Y.D., L.G., S.C., Lu.B. and D.E. produced and analysed the networks. E.K., C.B. and G.G. supervised the study. M.S., J.R., E.K., C.B. and G.G. provided constructive comments, revised and edited the manuscript. Tara Oceans coordinators provided constructive criticism throughout the study. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Lionel Guidi or Samuel Chaffron or Lucie Bittner or Damien Eveillard or Jeroen Raes or Eric Karsenti or Chris Bowler or Gabriel Gorsky.

Data described herein is available at European Nucleotide Archive under the project identifiers PRJEB402, PRJEB6610 and PRJEB7988, PANGAEA48,49,50, and a companion website ( The data release policy regarding future public release of Tara Oceans data is described in ref. 51.

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  1. 1.

    Supplementary Information

    This file contains Supplementary Tables 1-13. Supplementary Tables 11 and 12 were replaced on 7 March 2016 to include the sample IDs and ENA run accession numbers.

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  1. 1.

    Supplementary Information

    This file contains a full list of coordinators in the Tara Oceans Consortium. This file was updated on 12 February 2016 to correct some errors in the affiliations of members of the consortium.

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