Abstract

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

  • Corrected online 12 February 2016

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

Accessions

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European Nucleotide Archive

References

  1. 1.

    , , & Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998)

  2. 2.

    & Evidence of the potential influence of planktonic community structure on the interannual variability of particulate organic-carbon flux. Deep Sea Res. Part I Oceanogr. Res. Pap. 42, 619–639 (1995)

  3. 3.

    et al. Effects of phytoplankton community on production, size, and export of large aggregates: a world-ocean analysis. Limnol. Oceanogr. 54, 1951–1963 (2009)

  4. 4.

    , & The impact of remineralization depth on the air-sea carbon balance. Nature Geosci. 2, 630–635 (2009)

  5. 5.

    IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Cambridge University Press, 2013)

  6. 6.

    Biological robustness. Nature Rev. Genet. 5, 826–837 (2004)

  7. 7.

    , , & Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500, 449–452 (2013)

  8. 8.

    , , , & Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J. 8, 816–829 (2014)

  9. 9.

    Microbial community structure and its functional implications. Nature 459, 193–199 (2009)

  10. 10.

    et al. Determinants of community structure in the global plankton interactome. Science 348, (2015)

  11. 11.

    et al. Reconciliation of the carbon budget in the ocean’s twilight zone. Nature 507, 480–483 (2014)

  12. 12.

    Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694–696 (1998)

  13. 13.

    et al. Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump. Nature Commun. 6, 7608 (2015)

  14. 14.

    , & Massive fluxes of rhizosolenid diatoms – a common occurrence. Limnol. Oceanogr. 36, 1452–1457 (1991)

  15. 15.

    , & Diatom fluxes to the deep sea in the oligotrophic north Pacific gyre at station ALOHA. Mar. Ecol. Prog. Ser. 182, 55–67 (1999)

  16. 16.

    et al. Eddy-driven subduction exports particulate organic carbon from the spring bloom. Science 348, 222–225 (2015)

  17. 17.

    & Small phytoplankton and carbon export from the surface ocean. Science 315, 838–840 (2007)

  18. 18.

    et al. Bacterial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone. Limnol. Oceanogr. 53, 1327–1338 (2008)

  19. 19.

    Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog. Oceanogr. 130, 205–248 (2015)

  20. 20.

    et al. A holistic approach to marine eco-systems biology. PLoS Biol. 9, (2011)

  21. 21.

    Microbial ecology of ocean biogeochemistry: a community perspective. Science 320, 1043–1045 (2008)

  22. 22.

    et al. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347, 1257594 (2015)

  23. 23.

    et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015)

  24. 24.

    et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015)

  25. 25.

    et al. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015)

  26. 26.

    et al. Tara Oceans studies plankton at planetary scale. Science 348, 873 (2015)

  27. 27.

    , , & Particulate organic carbon fluxes to the ocean interior and factors controlling the biological pump: A synthesis of global sediment trap programs since 1983. Prog. Oceanogr. 76, 217–285 (2008)

  28. 28.

    , & Global patterns in efficiency of particulate organic carbon export and transfer to the deep ocean. Glob. Biogeochem. Cycles 26, (2012)

  29. 29.

    , , & A sparse PLS for variable selection when integrating omics data. Stat. Appl. Genet. Mol. Biol. 7, 35 (2008)

  30. 30.

    , , & A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res. 20, 947–959 (2010)

  31. 31.

    & Microbial interactions: from networks to models. Nature Rev. Microbiol. 10, 538–550 (2012)

  32. 32.

    et al. Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proc. Natl Acad. Sci. 112, 5443–5448 (2015)

  33. 33.

    & WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9 (2008)

  34. 34.

    , , , & Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre. Front. Microbiol. 6, (2015)

  35. 35.

    et al. Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment. PLoS ONE 3, (2008)

  36. 36.

    & Microbial structuring of marine ecosystems. Nature Rev. Microbiol. 5, 782–791 (2007)

  37. 37.

    , & Metatranscriptomics reveals unique microbial small RNAs in the ocean’s water column. Nature 459, 266–269 (2009)

  38. 38.

    et al. The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol. 5, e16 (2007)

  39. 39.

    Marine viruses – major players in the global ecosystem. Nature Rev. Microbiol. 5, 801–812 (2007)

  40. 40.

    Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181 (2004)

  41. 41.

    et al. Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32, 119–137 (2010)

  42. 42.

    & Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Glob. Change Biol. 17, 154–162 (2011)

  43. 43.

    et al. Climate-driven trends in contemporary ocean productivity. Nature 444, 752–755 (2006)

  44. 44.

    et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503 (2006)

  45. 45.

    et al. Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc. Natl Acad. Sci. USA 106, 1374–1379 (2009)

  46. 46.

    et al. The influence of functional diversity and composition on ecosystem processes. Science 277, 1300–1302 (1997)

  47. 47.

    et al. Genes to ecosystems: exploring the frontiers of ecology with one of the smallest biological units. New Phytol. 191, 19–36 (2011)

  48. 48.

    et al. Vertical profiles of environmental parameters measured on discrete water samples collected with Niskin bottles during the Tara Oceans expedition 2009-2013. PANGAEA (2014)

  49. 49.

    et al. Vertical profiles of environmental parameters measured from physical, optical and imaging sensors during Tara Oceans expedition 2009-2013. PANGAEA (2014)

  50. 50.

    et al. Contextual environmental data of selected samples from the Tara Oceans Expedition (2009–2013). PANGAEA (2014)

  51. 51.

    et al. Open science resources for the discovery and analysis of Tara Oceans data. Sci. Data 2, 150023 (2015)

  52. 52.

    et al. The Underwater Vision Profiler 5: An advanced instrument for high spatial resolution studies of particle size spectra and zooplankton. Limnol. Oceanogr. Methods 8, 462–473 (2010)

  53. 53.

    & Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997)

  54. 54.

    Size spectra and aggregation of suspended particles in the deep ocean. Deep Sea Res. Part I Oceanogr. Res. Pap. 31, 329–352 (1984)

  55. 55.

    , & Size distribution of particles in ocean. Limnol. Oceanogr. 17, 327–340 (1972)

  56. 56.

    et al.. Relationship between particle size distribution and flux in the mesopelagic zone. Deep Sea Res. Part I Oceanogr. Res. Pap. 55, 1364–1374 (2008)

  57. 57.

    et al. Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ. Microbiol. 16, 2659–2671 (2014)

  58. 58.

    et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013)

  59. 59.

    Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010)

  60. 60.

    et al. MOCAT: a metagenomics assembly and gene prediction toolkit. PLoS ONE 7, e47656 (2012)

  61. 61.

    et al. Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7, 1678–1695 (2013)

  62. 62.

    , & RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformatics 28, 125–126 (2012)

  63. 63.

    & Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357–359 (2012)

  64. 64.

    & Sparse principal component analysis via regularized low rank matrix approximation. J. Multivar. Anal. 99, 1015–1034 (2008)

  65. 65.

    & Eigengene networks for studying the relationships between co-expression modules. BMC Syst. Biol. 1, 54 (2007)

  66. 66.

    & Network neighborhood analysis with the multi-node topological overlap measure. Bioinformatics 23, 222–231 (2007)

  67. 67.

    & Performance of some variable selection methods when multicollinearity is present. Chemometr. Intell. Lab. 78, 103–112 (2005)

  68. 68.

    & The pls package: Principal component and partial least squares regression in R. J. Stat. Softw. 18, 1–23 (2007)

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Acknowledgements

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 (http://oceans.taraexpeditions.org). 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.

Affiliations

  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

Consortia

  1. Tara Oceans Consortium Coordinators

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

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Contributions

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 (http://www.raeslab.org/companion/ocean-carbon-export.html). The data release policy regarding future public release of Tara Oceans data is described in ref. 51.

Extended data

Supplementary information

Excel files

  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.

PDF files

  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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