Expression profiling of host and virus during a coccolithophore bloom provides insights into the role of viral infection in promoting carbon export

  • The ISME Journalvolume 12pages704713 (2018)
  • doi:10.1038/s41396-017-0004-x
  • Download Citation
Published online:


The cosmopolitan coccolithophore Emiliania huxleyi is a unicellular eukaryotic alga that forms vast blooms in the oceans impacting large biogeochemical cycles. These blooms are often terminated due to infection by the large dsDNA virus, E. huxleyi virus (EhV). It was recently established that EhV-induced modulation of E. huxleyi metabolism is a key factor for optimal viral infection cycle. Despite the huge ecological importance of this host–virus interaction, the ability to assess its spatial and temporal dynamics and its possible impact on nutrient fluxes is limited by current approaches that focus on quantification of viral abundance and biodiversity. Here, we applied a host and virus gene expression analysis as a sensitive tool to quantify the dynamics of this interaction during a natural E. huxleyi bloom in the North Atlantic. We used viral gene expression profiling as an index for the level of active infection and showed that the latter correlated with water column depth. Intriguingly, this suggests a possible sinking mechanism for removing infected cells as aggregates from the E. huxleyi population in the surface layer into deeper waters. Viral infection was also highly correlated with induction of host metabolic genes involved in host life cycle, sphingolipid, and antioxidant metabolism, providing evidence for modulation of host metabolism under natural conditions. The ability to track and quantify defined phases of infection by monitoring co-expression of viral and host genes, coupled with advance omics approaches, will enable a deeper understanding of the impact that viruses have on the environment.

  • Subscribe to The ISME Journal for full access:



Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.


  1. 1

    Breitbart M. Marine viruses: truth or dare. Ann Rev Mar Sci. 2012;4:425–48.

  2. 2

    Rohwer F, Thurber RV. Viruses manipulate the marine environment. Nature. 2009;459:207–12.

  3. 3

    Suttle Ca. Marine viruses—major players in the global ecosystem. Nat Rev Microbiol. 2007;5:801–12.

  4. 4

    Wilhelm SW, Suttle CA. Viruses and nutrient cycles in the sea. Bioscience. 1999;49:781.

  5. 5

    Forterre P. The virocell concept and environmental microbiology. ISME J. 2013;7:233–6.

  6. 6

    Rosenwasser S, Ziv C, Creveld SG, van, Vardi A. Virocell metabolism: metabolic innovations during host–virus interactions in the ocean. Trends Microbiol. 2016;24:821–32.

  7. 7

    Mojica KDA, Huisman J, Wilhelm SW, Brussaard CPD. Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean. ISME J. (2015) 10; 500–513.

  8. 8

    Sheik AR, Brussaard CPD, Lavik G, Lam P, Musat N, Krupke A, et al. Responses of the coastal bacterial community to viral infection of the algae Phaeocystis globosa. ISME J. 2013;8:1–14.

  9. 9

    Bidle KD, Vardi A. A chemical arms race at sea mediates algal host-virus interactions. Curr Opin Microbiol. 2011;14:449–57.

  10. 10

    Brown CW, Yoder JA. Coccolithophorid blooms in the global ocean. J Geophys Res Ocean. 1994;99:7467–82.

  11. 11

    Holligan PM, Viollier M, Harbour DS, Camus P, Champagne-Philippe M. Satellite and ship studies of coccolithophore production along a continental shelf edge. Nature. 1983;304:339–42.

  12. 12

    Balch WM, Holligan PM, Kilpatrick Ka. Calcification, photosynthesis and growth of the bloom-forming coccolithophore, Emiliania huxleyi. Cont Shelf Res. 1992;12:1353–74.

  13. 13

    Winter A, Henderiks J, Beaufort L, Rickaby REM, Brown CW. Poleward expansion of the coccolithophore Emiliania huxleyi. J Plankton Res. 2014;36:316–25.

  14. 14

    Bolton CT, Hernández-Sánchez MT, Fuertes M-Á, González-Lemos S, Abrevaya L, Mendez-Vicente A, et al. Decrease in coccolithophore calcification and CO2 since the middle Miocene. Nat Commun. 2016;7:10284.

  15. 15

    Gal A, Wirth R, Kopka J, Fratzl P, Faivre D, Scheffel A. Macromolecular recognition directs calcium ions to coccolith mineralization sites. Science. 2016;353:590–3.

  16. 16

    Rost B, Riebesell U. Coccolithophores and the biological pump: responses to environmental changes. In: Thierstein HR, Young JR, editors. Coccolithophores. Berlin, Heidelberg: Springer; 2004. p. 99–125.

  17. 17

    Alcolombri U, Ben-Dor S, Feldmesser E, Levin Y, Tawfik DS, Vardi A. Identification of the algal dimethyl sulfide-releasing enzyme: A missing link in the marine sulfur cycle. Science. 2015;348:1466–9.

  18. 18

    Simó R. Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol. 2001;16:287–94.

  19. 19

    Highfield A, Evans C, Walne A, Miller PI, Schroeder DC. How many Coccolithovirus genotypes does it take to terminate an Emiliania huxleyi bloom? Virology. 2014;466-467:138–45.

  20. 20

    Lehahn Y, Koren I, Schatz D, Frada M, Sheyn U, Boss E, et al. Decoupling physical from biological processes to assess the impact of viruses on a mesoscale algal bloom. Curr Biol. 2014b;24:2041–6.

  21. 21

    Martínez JM, Schroeder DC, Wilson WH. Dynamics and genotypic composition of Emiliania huxleyi and their co-occurring viruses during a coccolithophore bloom in the North Sea. FEMS Microbiol Ecol. 2012;81:315–23.

  22. 22

    Vardi A, Haramaty L, Van Mooy BaS, Fredricks HF, Kimmance Sa, Larsen A, et al. Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc Natl Acad Sci USA. 2012;109:19327–32.

  23. 23

    Allen MJ, Forster T, Schroeder DC, Hall M, Roy D, Ghazal P, et al. Locus-specific gene expression pattern suggests a unique propagation strategy for a giant algal virus. J Virol. 2006;80:7699–705.

  24. 24

    Rosenwasser S, Mausz MAMA, Schatz D, Sheyn U, Malitsky S, Aharoni A, et al. Rewiring host lipid metabolism by large viruses determines the fate of emiliania huxleyi, a bloom-forming alga in the ocean. Plant Cell. 2014;26:2689–707.

  25. 25

    Wilson WH, Schroeder DC, Allen MJ, Holden MTG, Parkhill J, Barrell BG, et al. Complete genome sequence and lytic phase transcription profile of a coccolithovirus. Science. 2005;309:1090–2.

  26. 26

    Malitsky S, Ziv C, Rosenwasser S, Zheng S, Schatz D, Porat Z, et al. Viral infection of the marine alga Emiliania huxleyi triggers lipidome remodeling and induces the production of highly saturated triacylglycerol. New Phytol. 2016;210:88–96.

  27. 27

    Schatz D, Shemi A, Rosenwasser S, Sabanay H, Wolf SG, Ben-Dor S, et al. Hijacking of an autophagy-like process is critical for the life cycle of a DNA virus infecting oceanic algal blooms. New Phytol. 2014;204:854–63.

  28. 28

    Sheyn U, Rosenwasser S, Ben-Dor S, Porat Z, Vardi A. Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. ISME J. 2016;10:1742–54.

  29. 29

    Ziv C, Malitsky S, Othman A, Ben-Dor S, Wei Y, Zheng S, 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. 2016;113:E1907–E1916.

  30. 30

    Fulton JM, Fredricks HF, Bidle KD, Vardi A, Kendrick BJ, Ditullio GR, et al. Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ Microbiol. 2013;16: 1137–49.

  31. 31

    Vardi A, Van Mooy BAS, Fredricks HF, Popendorf KJ, Ossolinski JE, Haramaty L, et al. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science. 2009;326:861–5.

  32. 32

    Brussaard CPD. Optimization of procedures for counting viruses by flow cytometry. Appl Environ Microbiol. 2004;70:1506–13.

  33. 33

    Coolen MJL. 7000 years of Emiliania huxleyi viruses in the Black Sea. Science. 2011;333:451–2.

  34. 34

    Frada MJ, Schatz D, Farstey V, Ossolinski JE, Sabanay H, Ben-Dor S, et al. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr Biol. 2014;24:2592–7.

  35. 35

    Schroeder DC, Oke J, Hall M, Malin G, Wilson WH. Virus succession observed during an Emiliania huxleyi bloom. Appl Environ Microbiol. 2003;69:2484–90.

  36. 36

    Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, et al. Ocean plankton. Patterns and ecological drivers of ocean viral communities. Science. 2015;348:1261498.

  37. 37

    Culley AI, Lang AS, Suttle CA. Metagenomic analysis of coastal RNA virus communities. Science. 2006;312:1795–8.

  38. 38

    Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, et al. The marine viromes of four oceanic regions. PLoS Biol. 2006;4:e368.

  39. 39

    Schroeder DC, Oke J, Malin G, Wilson WH. Coccolithovirus (Phycodnaviridae): characterisation of a new large dsDNA algal virus that infects Emiliana huxleyi. Arch Virol. 2002;147:1685–98.

  40. 40

    Bendif EM, Probert I, Carmichael M, Romac S, Hagino K, de Vargas C. Genetic delineation between and within the widespread coccolithophore morpho-species Emiliania huxleyi and Gephyrocapsa oceanica (Haptophyta). J Phycol. 2014;50:140–8.

  41. 41

    Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005;12:1047–64.

  42. 42

    Brown C. Global distribution of coccolithophore blooms. Oceanography. 1995;8:59–60.

  43. 43

    Sharoni S, Trainic M, Schatz D, Lehahn Y, Flores MJ, Bidle KD, et al. Infection of phytoplankton by aerosolized marine viruses. Proc Natl Acad Sci USA. 2015;112:6643–7.

  44. 44

    Siegel H, Ohde T, Gerth M, Lavik G, Leipe T. Identification of coccolithophore blooms in the SE Atlantic Ocean off Namibia by satellites and in-situ methods. Cont Shelf Res. 2007;27:258–74.

  45. 45

    Tyrrell T, Merico A. Emiliania huxleyi: bloom observations and the conditions that induce them. In: Thierstein HR, Young JR, editors. Coccolithophores. Berlin, Heidelberg: Springer; 2004. p. 75–97.

  46. 46

    Lehahn Y, Koren I, Rudich Y, Bidle KD, Trainic M, Flores JM, et al. Decoupling atmospheric and oceanic factors affecting aerosol loading over a cluster of mesoscale North Atlantic eddies. Geophys Res Lett. 2014;41:4075–81.

  47. 47

    Ledwell JR, McGillicuddy DJ, Anderson LA. Nutrient flux into an intense deep chlorophyll layer in a mode-water eddy. Deep Sea Res Part II Top Stud Oceanogr. 2008;55:1139–60.

  48. 48

    McGillicuddy DJ, Anderson LA, Bates NR, Bibby T, Buesseler KO, Carlson CA, et al. Eddy/wind interactions stimulate extraordinary mid-ocean plankton blooms. Science. 2007;316:1021–6.

  49. 49

    Holligan PM, Fernández E, Aiken J, Balch WM, Boyd P, Burkill PH, et al. A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic. Glob Biogeochem Cycles. 1993;7:879–900.

  50. 50

    Townsend DW, Keller MD, Holligan PM, Ackleson SG, Balch WM. Blooms of the coccolithophore Emiliania huxleyi with respect to hydrography in the Gulf of Maine. Cont Shelf Res. 1994;14:979–1000.

  51. 51

    Wilson WH, Tarran GA, Schroeder D, Cox M, Oke J, Malin G. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J Mar Biol Assoc UK. 2002;82:369–77.

  52. 52

    Cokacar T, Kubilay N, Oguz T. Structure of Emiliania huxleyi blooms in the Black Sea surface waters as detected by SeaWIFS imagery. Geophys Res Lett. 2001;28:4607–10.

  53. 53

    Berge G. Discoloration of the sea due to Coccolithus huxleyi ‘bloom’. Sarsia. 1962;6:27–40.

  54. 54

    Brussaard CPD, Payet JP, Winter C, Weinbauer MG. Quantification of aquatic viruses by flow cytometry Wilhelm S, Weinbauer M, Suttle C (eds). Man Aquat Viral Ecol. 2010;11:102–9.

  55. 55

    Mari X, Kerros M-E, Weinbauer MG. Virus attachment to transparent exopolymeric particles along trophic gradients in the southwestern lagoon of New Caledonia. Appl Environ Microbiol. 2007;73:5245–52.

  56. 56

    Azetsu-Scott K, Passow U. Ascending marine particles: significance of transparent exopolymer particles (TEP) in the upper ocean. Limnol Oceanogr 2004;49:741–8.

  57. 57

    Harlay J, De Bodt C, Engel A, Jansen S, D’Hoop Q, Piontek J, et al. Abundance and size distribution of transparent exopolymer particles (TEP) in a coccolithophorid bloom in the northern Bay of Biscay. Deep Sea Res Part I Oceanogr Res Pap. 2009;56:1251–65.

  58. 58

    Schmidt S, Harlay J, Borges AV, Groom S, Delille B, Roevros N, et al. Particle export during a bloaom of Emiliania huxleyi in the North-West European continental margin. J Mar Syst. 2013;109-110:S182–S190.

  59. 59

    Francois R, Honjo S, Krishfield R, Manganini S. Factors controlling the flux of organic carbon to the bathypelagic zone of the ocean. Glob Biogeochem Cycles. 2002;16:34-1–34–20.

  60. 60

    Iversen MH, Ploug H. Ballast minerals and the sinking carbon flux in the ocean: Carbon-specific respiration rates and sinking velocity of marine snow aggregates. Biogeosciences. 2010;7:2613–24.

  61. 61

    Klaas C, Archer DE. Association of sinking organic matter with various types of mineral ballast in the deep sea: Implications for the rain ratio. Glob Biogeochem Cycles. 2002;16:63–1-63–14.

  62. 62

    Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature. 2016;532:465–70.

  63. 63

    Lawrence JJE, Suttle CA. Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat Microb Ecol. 2004;37:1–7.

  64. 64

    Balch WM, Kilpatrick KA, Trees CC. The 1991 coccolithophore bloom in the central North Atlantic. 1. Optical properties and factors affecting their distribution. Limnol Oceanogr. 1996;41:1669–83.

  65. 65

    Collins JR, Edwards BR, Thamatrakoln K, Ossolinski JE, DiTullio GR, Bidle KD, et al. The multiple fates of sinking particles in the North Atlantic Ocean. Glob Biogeochem Cycles. 2015;29:1471–94.

  66. 66

    Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature. 2016;537:689–93.

  67. 67

    Schlitzer R. Interactive analysis and visualization of geoscience data with Ocean Data View. Comput Geosci. 2002;28:1211–8.

  68. 68

    Spitzer M, Wildenhain J, Rappsilber J, Tyers M. BoxPlotR: a web tool for generation of box plots. Nat Methods. 2014;11:121–2.

Download references


We thank the captain and crew of the R/V Knorr during the NAVICE cruise as well as the Marine Facilities and Operations at the Woods Hole Oceanographic Institution for assistance and cooperation at sea. We thank Shifra Ben-Dor for her contribution to the bioinformatics analysis. This research was supported by a European Research Council (ERC) StG (INFOTROPHIC grant # 280991) and CoG (VIROCELLSPHERE grant # 681715) as well as by the National Science Foundation (NSF) grant OCE-1061883 (to AV and KDB).

Author Contributions

US, SR, and AV conceived and design the experiments and analyses. US and SR analyzed the expression data. DS and NBG preformed and analyzed E. huxleyi and viral DNA qPCR enumeration. US analyzed all data including the cruise data. YL and IK analyzed satellite imagery. KDB was the chief scientist on the NAVICE cruise and implemented corresponding ship-based sampling strategies. RR preformed statistical analysis. US, AV, NBG, SR, and DS contributed to the writing of the manuscript. AV supervised the project.

Author information


  1. Departments of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel

    • Uri Sheyn
    • , Shilo Rosenwasser
    • , Noa Barak-Gavish
    • , Daniella Schatz
    •  & Assaf Vardi
  2. The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University, Rehovot, 7610001, Israel

    • Shilo Rosenwasser
  3. Departments of Earth and Planetary Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel

    • Yoav Lehahn
    •  & Ilan Koren
  4. Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, 7610001, Israel

    • Ron Rotkopf
  5. Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, 08901, USA

    • Kay D. Bidle


  1. Search for Uri Sheyn in:

  2. Search for Shilo Rosenwasser in:

  3. Search for Yoav Lehahn in:

  4. Search for Noa Barak-Gavish in:

  5. Search for Ron Rotkopf in:

  6. Search for Kay D. Bidle in:

  7. Search for Ilan Koren in:

  8. Search for Daniella Schatz in:

  9. Search for Assaf Vardi in:

Conflict of interest

The authors declare no conflict of interest.

Corresponding author

Correspondence to Assaf Vardi.

Electronic supplementary material