Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Coccolithovirus facilitation of carbon export in the North Atlantic

Nature Microbiology volume 3, pages 537–547 (2018)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: MODIS/Aqua (1 km resolution)-derived near-surface PIC and Chl a concentration images of water mass features containing E. huxleyi blooms in the North Atlantic.
Fig. 2: Natural populations at different stages of EhV infection have distinct in situ optical properties.
Fig. 3: Diagnosis of virus infection using lipid- and DNA-based biomolecular proxies.
Fig. 4: Active EhV infection triggers TEP-facilitated aggregation, POC export and remineralization in the mesopelagic.

Similar content being viewed by others

References

  1. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Weitz, J. S. et al. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J. 9, 1352 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Rousseaux, C. S. & Gregg, W. W. Interannual variation in phytoplankton primary production at a global scale. Remote Sens. 6, 1–19 (2013).

    Article  Google Scholar 

  4. Berelson, W. et al. Relating estimates of CaCO3 production, export, and dissolution in the water column to measurements of CaCO3 rain into sediment traps and dissolution on the sea floor: a revised global carbonate budget. Global Biogeochem. Cycles 21, GB1024 (2007).

    Article  Google Scholar 

  5. Tyrrell, T. & Merico, A. in Coccolithophores (eds Thierstein, H. R. & Young, J. R.) 75–97 (Springer, Berlin, 2004).

  6. Bratbak, G., Egge, J. K. & Heldal, M. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93, 39–48 (1993).

    Article  Google Scholar 

  7. Vardi, A. et al. Host–virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc. Natl Acad. Sci. USA 109, 19327–19332 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Lehahn, Y. et al. Decoupling physical from biological processes to assess the impact of viruses on a mesoscale algal bloom. Curr. Biol. 24, 2041–2046 (2014).

    Article  CAS  PubMed  Google Scholar 

  9. Schatz, D. et al. Hijacking of an autophagy-like process is critical for the life cycle of a DNA virus infecting oceanic algal blooms. New Phytol. 204, 854–863 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Vardi, A. et al. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326, 861–865 (2009).

    Article  CAS  PubMed  Google Scholar 

  11. Bidle, K. D., Haramaty, L., e Ramos, J. B. & Falkowski, P. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc. Natl Acad. Sci. USA 104, 6049–6054 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ziv, C. et al. Viral serine palmitoyltransferase induces metabolic switch in sphingolipid biosynthesis and is required for infection of a marine alga. Proc. Natl Acad. Sci. USA 113, E1907–E1916 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fulton, J. M. et al. Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ. Microbiol. 16, 1137–1149 (2014).

    Article  CAS  PubMed  Google Scholar 

  14. Hunter, J. E., Frada, M. J., Fredricks, H. F., Vardi, A. & Van Mooy, B. A. Targeted and untargeted lipidomics of Emiliania huxleyi viral infection and life cycle phases highlights molecular biomarkers of infection, susceptibility, and ploidy. Front. Mar. Sci. 2, 81 (2015).

    Article  Google Scholar 

  15. Bidle, K. D. The molecular ecophysiology of programmed cell death in marine phytoplankton. Annu. Rev. Mar. Sci. 7, 341–375 (2015).

    Article  Google Scholar 

  16. Castillo, C. R., Sarmento, H., Alvarez-Salgado, X. A., Gasol, J. M. & Marraséa, C. Production of chromophoric dissolved organic matter by marine phytoplankton. Limnol. Oceanogr. 55, 446–454 (2010).

    Article  Google Scholar 

  17. Passow, U. & Alldredge, A. L. Do transparent exopolymer particles (TEP) inhibit grazing by the euphausiid Euphausia pacifica? J. Plankton Res. 21, 2203–2217 (1999).

    Article  CAS  Google Scholar 

  18. Evans, C. & Wilson, W. H. Preferential grazing of Oxyrrhis marina on virus infected Emiliania huxleyi. Limnol. Oceanogr. 53, 2035–2040 (2008).

    Article  Google Scholar 

  19. Briggs, N. et al. High-resolution observations of aggregate flux during a sub-polar North Atlantic spring bloom. Deep Sea Res. I Oceanogr. Res. Pap. 58, 1031–1039 (2011).

    Article  Google Scholar 

  20. Frada, M. J. et al. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr. Biol. 24, 2592–2597 (2014).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Collins, J. R. et al. The multiple fates of sinking particles in the North Atlantic Ocean. Glob. Biogeochem. Cycles 29, 1471–1494 (2015).

    Article  CAS  Google Scholar 

  23. Denman, K. & Gargett, A. Biological–physical interactions in the upper ocean: the role of vertical and small scale transport processes. Annu. Rev. Fluid Mech. 27, 225–256 (1995).

    Article  Google Scholar 

  24. Sheyn, U. et al. Expression profiling of host and virus during a coccolithophore bloom provides insights into the role of viral infection in promoting carbon export. ISME J. https://doi.org/10.1038/s41396-017-0004-x (2018).

  25. Azetsu-Scott, K. & Passow, U. Ascending marine particles: significance of transparent exopolymer particles (TEP) in the upper ocean. Limnol. Oceanogr. 49, 741–748 (2004).

    Article  CAS  Google Scholar 

  26. Alldredge, A. L., Passow, U. & Haddock, H. The characteristics and transparent exopolymer particle (TEP) content of marine snow formed from thecate dinoflagellates. J. Plankton Res. 20, 393–406 (1998).

    Article  Google Scholar 

  27. Morison, F. & Menden-Deuer, S. Early spring phytoplankton dynamics in the subpolar North Atlantic: the influence of protistan herbivory. Limnol. Oceanogr. 60, 1298–1313 (2015).

    Article  Google Scholar 

  28. Vermont, A. et al. Virus infection of Emiliania huxleyi deters grazing by the copepod Acartia tonsa. J. Plankton Res. 38, 1194–1205 (2016).

    Article  Google Scholar 

  29. Harris, R. Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol. 119, 431–439 (1994).

    Article  Google Scholar 

  30. Guidi, L. et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465–470 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Martz, T. R., Johnson, K. S. & Riser, S. C. Ocean metabolism observed with oxygen sensors on profiling floats in the South Pacific. Limnol. Oceanogr. 53, 2094–2111 (2008).

    Article  CAS  Google Scholar 

  32. Anderson, L. A. & Sarmiento, J. L. Redfield ratios of remineralization determined by nutrient data analysis. Glob. Biogeochem. Cycles 8, 65–80 (1994).

    Article  CAS  Google Scholar 

  33. McDonnell, A. M. & Buesseler, K. O. A new method for the estimation of sinking particle fluxes from measurements of the particle size distribution, average sinking velocity, and carbon content. Limnol. Oceanogr. 10, 329–346 (2012).

    Article  Google Scholar 

  34. Peterson, M. L., Wakeham, S. G., Lee, C., Askea, M. A. & Miquel, J. C. Novel techniques for collection of sinking particles in the ocean and determining their settling rates. Limnol. Oceanogr. Methods 3, 520–532 (2005).

    Article  CAS  Google Scholar 

  35. Lamborg, C. et al. The flux of bio- and lithogenic material associated with sinking particles in the mesopelagic “twilight zone” of the northwest and North Central Pacific Ocean. Deep Sea Res. II Top. Stud. Oceanogr. 55, 1540–1563 (2008).

    Article  Google Scholar 

  36. Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).

    Article  CAS  PubMed  Google Scholar 

  37. Popendorf, K. J., Fredricks, H. F. & Van Mooy, B. A. Molecular ion-independent quantification of polar glycerolipid classes in marine plankton using triple quadrupole MS. Lipids 48, 185–195 (2013).

    Article  CAS  PubMed  Google Scholar 

  38. Coolen, M. J. L. 7000 years of Emiliania huxleyi viruses in the Black Sea. Science 333, 451–452 (2011).

    Article  CAS  PubMed  Google Scholar 

  39. Kolber, Z. S., Prášil, O. & Falkowski, P. G. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim. Biophys. Acta 1367, 88–106 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Landry, M. & Hassett, R. Estimating the grazing impact of marine micro-zooplankton. Mar. Biol. 67, 283–288 (1982).

    Article  Google Scholar 

  41. Evans, C., Archer, S. D., Jacquet, S. & Wilson, W. H. Direct estimates of the contribution of viral lysis and microzooplankton grazing to the decline of a Micromonas spp. population. Aquat. Microb. Ecol. 30, 207–219 (2003).

    Article  Google Scholar 

  42. Welschmeyer, N. A. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr. 39, 1985–1992 (1994).

    Article  CAS  Google Scholar 

  43. Zapata, M., Rodríguez, F. & Garrido, J. L. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar. Ecol. Progress. Ser. 195, 29–45 (2000).

    Article  CAS  Google Scholar 

  44. DiTullio, G. & Geesey, M. E. in Encyclopedia of Environmental Microbiology (ed. Bitton, G.) 2453–2470 (Wiley, New York, 2002).

  45. Mackey, M., Mackey, D., Higgins, H. & Wright, S. CHEMTAX—a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar. Ecol. Progress. Ser. 144, 265–283 (1996).

    Article  CAS  Google Scholar 

  46. Nissimov, J. I. et al. Draft genome sequence of four coccolithoviruses: Emiliania huxleyi virus EhV-88, EhV-201, EhV-207, and EhV-208. J. Virol. 86, 2896–2897 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Brussaard, C. P., Payet, J. P., Winter, C. & Weinbauer, M. G. Quantification of aquatic viruses by flow cytometry. Man. Aquat. Viral Ecol. 11, 102–107 (2010).

    Article  Google Scholar 

  48. Siegel, D. A., Fields, E. & Buesseler, K. O. A bottom-up view of the biological pump: modeling source funnels above ocean sediment traps. Deep Sea Res. I Oceanogr. Res. Pap. 55, 108–127 (2008).

    Article  Google Scholar 

  49. Ploug, H., Iversen, M. H., Koski, M. & Buitenhuis, E. T. Production, oxygen respiration rates, and sinking velocity of copepod fecal pellets: direct measurements of ballasting by opal and calcite. Limnol. Oceanogr. 53, 469–476 (2008).

    Article  CAS  Google Scholar 

Download references

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

  1. Filipa Carvalho

    Present address: National Oceanography Centre, Southampton, United Kingdom

  2. Miguel Frada

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

  3. Rebecca Vandzura

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

  4. Yoav Lehahn

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

Authors and 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

Authors
  1. Christien P. Laber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan E. Hunter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Filipa Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James R. Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elias J. Hunter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brittany M. Schieler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Emmanuel Boss
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kuldeep More
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Miguel Frada
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kimberlee Thamatrakoln
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Christopher M. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Liti Haramaty
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Justin Ossolinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Helen Fredricks
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jozef I. Nissimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Rebecca Vandzura
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Uri Sheyn
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Yoav Lehahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Robert J. Chant
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Ana M. Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Marco J. L. Coolen
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Assaf Vardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Giacomo R. DiTullio
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Benjamin A. S. Van Mooy
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Kay D. Bidle
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Kay D. Bidle.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–15, Supplementary Figures 1–3, Supplementary References.

Life Sciences Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Laber, C.P., Hunter, J.E., Carvalho, F. et al. Coccolithovirus facilitation of carbon export in the North Atlantic. Nat Microbiol 3, 537–547 (2018). https://doi.org/10.1038/s41564-018-0128-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology