Abstract

Marine phytoplankton account for approximately half of global primary productivity1, making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon2, which can stimulate nutrient regeneration, primary production and upper ocean respiration2 via lytic infection and the ‘virus shunt’. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean2. Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid- and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in ‘early-infected blooms’ with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

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Acknowledgements

We thank the captain and crew of the RV Knorr for assistance and cooperation at sea, as well as Marine Facilities and Operations at the Woods Hole Oceanographic Institution for logistical support. We thank R. Fernandes and S. Prakya (University of the Azores) and I. Bashmachnikov (Saint Petersburg University) for daily downloading and sending MODIS and AVISO altimetry data to the RV Knorr for onboard processing. We also thank B. Edwards for logistical help with sediment trap deployments and recoveries. R. Stevens (College of Charleston) and A. Neeley (NASA) provided assistance with the dilution experiments and CHEMTAX analyses, respectively. This study was supported by grants from the National Science Foundation to K.D.B. (OCE-1061876, OCE-1537951 and OCE-1459200), M.J.L.C., G.R.D., A.V. and B.A.S.V.M. (OCE-1050995), and R.J.C. and E.J.H. (OCE-1325258), and from the Gordon and Betty Moore Foundation to K.D.B. (GBMF3789) and B.A.S.V.M. (GBMF3301).

Author information

Author notes

    • Filipa Carvalho

    Present address: National Oceanography Centre, Southampton, United Kingdom

    • Miguel Frada

    Present address: The Interuniversity Institute for Marine Sciences—Eilat, Eilat, Israel

    • Rebecca Vandzura

    Present address: College of Earth, Ocean and Environment, University of Delaware, Newark, DE, USA

    • Yoav Lehahn

    Present address: Department of Marine Geosciences, University of Haifa, Haifa, Israel

Affiliations

  1. Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, USA

    • Christien P. Laber
    • , Filipa Carvalho
    • , Elias J. Hunter
    • , Brittany M. Schieler
    • , Kimberlee Thamatrakoln
    • , Christopher M. Brown
    • , Liti Haramaty
    • , Jozef I. Nissimov
    • , Rebecca Vandzura
    • , Robert J. Chant
    •  & Kay D. Bidle
  2. Department of Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    • Jonathan E. Hunter
    • , James R. Collins
    • , Justin Ossolinski
    • , Helen Fredricks
    •  & Benjamin A. S. Van Mooy
  3. School of Marine Sciences, University of Maine, Walpole, ME, USA

    • Emmanuel Boss
  4. Western Australian Organic and Isotope Geochemistry Center, Department of Chemistry, Curtin University, Bentley, WA, Australia

    • Kuldeep More
    •  & Marco J. L. Coolen
  5. Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel

    • Miguel Frada
    • , Uri Sheyn
    • , Yoav Lehahn
    •  & Assaf Vardi
  6. Department of Oceanography and Fisheries, University of the Azores, Faial, Azores, Portugal

    • Ana M. Martins
  7. Grice Marine Laboratory, College of Charleston, Charleston, SC, USA

    • Giacomo R. DiTullio

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Contributions

C.P.L. operated the vertical profiling floats, processed the PIC, POC and nutrient samples, analysed and interpreted the bio-optical, lipid, genetic, flow cytometry, SEM, HPLC pigment, nutrient, Fv/Fm and TEP data, and wrote the manuscript. J.E.H. processed, analysed and interpreted the lipid samples and data, and provided extensive manuscript feedback. F.C. processed the MODIS/Aqua satellite data. J.R.C. helped with deployment and recovery of the sediment traps, analysed the sediment PIC and POC flux data, and provided extensive manuscript feedback. E.H. performed statistical particle funnel analyses and overlaid data onto the satellite imagery. B.M.S. processed, organized, and helped analyse the flow cytometry data, and also helped process nutrient samples. E.B. aided in vertical profile float mission planning, and processing and interpreting of the bio-optical data. K.M. performed qPCR for MCP and COI quantification. M.F. collected the SEM samples and provided extensive manuscript feedback. K.T. collected nutrient samples, analysed the Fv/Fm data and provided extensive manuscript feedback. C.M.B. collected and processed the flow cytometry samples. L.H. collected and processed the TEP samples, and organized the TEP and Fv/Fm data. J.O. led the operational deployment and recovery of the sediment traps. H.F. processed the GSL lipid data. U.S. collected and processed the flow cytometry data. J.I.N. designed the laboratory-based experiments and performed analyses of TEP production and particle dynamics. R.V. performed the laboratory-based experiments and helped with the analyses of TEP production and particle dynamics. Y.L. collected and processed the hindcast satellite data at the LI station. R.J.C. helped with analysis of the ADCP data, sediment trap trajectories and statistical particle funnel analysis. A.M.M. acquired, interpreted and processed the MODIS/Aqua Chl a, PIC, Rrs 555 and Rrs 547 data during the NA-VICE field campaign. M.J.L.C. was a co-investigator during the NA-VICE cruise, and collected and processed DNA samples for MCP and COI quantification. A.V. was a co-investigator during the NA-VICE cruise and collected nutrient samples. G.R.D. was a co-investigator during the NA-VICE cruise, collected and processed Chl a and HPLC pigment data, and analysed pigment data in CHEMTAX. B.A.S.V.M. was a co-investigator during the NA-VICE cruise, oversaw lipid analysis and sediment flux measurements, and provided extensive discussion and feedback throughout the investigation and during manuscript preparation. K.D.B. obtained funding support for the work, was chief scientist on the NA-VICE cruise, aided in interpreting the results and provided intellectual guidance in all aspects of the study. All authors read and approved the final manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Kay D. Bidle.

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https://doi.org/10.1038/s41564-018-0128-4

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