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A minireview of marine algal virus — Coccolithoviruses

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Abstract

Coccolithophorid is unicellular marine microalgae with a global distribution in temperate and sub-temperate oceanic regions and has the ability to produce ‘the coccoliths’. It is considered to be the second most productive calcifying organism on earth and becoming an important factor in the global carbonate cycle. Emiliania huxleyi is one of the only two bloom-forming coccolithophores and becomes a species crucial to the study of global biogeochemical cycles and climate modeling. Coccolithoviruse is a recently discovered group of viruses infecting the marine coccolithophorid E. huxleyi. They are a major cause of coccolithophore bloom termination, and DMSP concentration is increasing in the process of viral lysis. Phylogenetic evidences support that some genes are functional both in E. huxleyi and its virus (EhV). Horizontal gene transfer (HGT) of multiple functionally coupled enzymes occurs in E. huxleyi and its DNA virus EhV has been confirmed, which contributes to the diversification and adaptation of plankton in the oceans and also critically regulates virus-host infection by allowing viruses to control host metabolic pathways for their replication. Therefore, it is of particular interest to understand this host-virus interaction. On this issue, we have made a minireview of coccolithoviruses focusing on the basic characteristics, phylogenesis, horizontal gene transfer and the interaction between the host and its viruses, as well as its important role in global biogeochemical cycling.

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References

  • Allen, M. J., Lanzén, A., and Bratbak, G., 2011. Characterisation of the coccolithovirus intein. Marine Genomics, 4(1): 1–7.

    Article  Google Scholar 

  • Allen, M. J., Schroeder, D. C., Donkin, A., Crawfurd, K. J., and Wilson, W. H., 2006. Genome comparison of two Coccolithoviruses. Virology Journal, 3: 15, DOI: 10.1186/1743-422X-3-15.

    Article  Google Scholar 

  • Arnold, H. E., Kerrison, P., and Steinke, M., 2013. Interacting effects of ocean acidification and warming on growth and DMS-production in the haptophyte coccolithophore Emiliania huxleyi. Global Change Biology, 19(4): 1007–1016.

    Article  Google Scholar 

  • Bach, L. T., Mackinder, L. C., Schulz, K. G., Wheeler, G., Schroeder, D. C., Brownlee, C., and Riebesell, U., 2013. Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytologist, 199(1): 121–134.

    Article  Google Scholar 

  • Bates, N. R., Michaels, A. F., and Knap, A. H., 1996. Alkalinity changes in the Sargasso Sea; geochemical evidence of calcification?. Marine Chemistry, 51: 347–358.

    Article  Google Scholar 

  • Bates, T. S., Lamb, B. K., Guenther, A., Dignon, A., and Stoiberet, R. E., 1992. Sulfur emissions to the atmosphere from natural sources. Journal of Atmospheric Chemistry, 14: 315–337.

    Article  Google Scholar 

  • Bell, P. J., 2001. Viral eukaryogenesis: Was the ancestor of the nucleus a complex DNA virus? Journal of Molecular Evolution, 53(3): 251–256.

    Article  Google Scholar 

  • Bidle, K. D., 2007. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. PNAS Proceedings of the National Academy of Sciences of the United States of America, 104(14): 6049–6054.

    Article  Google Scholar 

  • Bidle, K. D., and Vardi, A., 2011. A chemical arms race at sea mediates algal host-virus interactions. Current Opinion in Microbiology, 14(4): 449–457.

    Article  Google Scholar 

  • Bratbak, G., Egge, J. K., and Heldal, M., 1993. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Marine Ecology-Progress Series, 93(1–2): 39–48.

    Article  Google Scholar 

  • Bratbak, G., Wilson, W., and Heldal, M., 1996. Viral control of Emiliania huxleyi blooms? Journal of Marine Systems, 9(1–2): 75–81.

    Article  Google Scholar 

  • Brussaard, C. P. D., Kempers, R. S., Kop, A. J., Riegman, R., and Heldal, M., 1996a. Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquatic Microbiology Ecology, 10: 105–113.

    Article  Google Scholar 

  • Brussaard, C. P. D., 2004. Viral control of phytoplankton populationsa Review. Journal of Eukaryotic Microbiology, 51(2): 125–138.

    Article  Google Scholar 

  • Cai, Y. Q., Zhang, Z. L., Luo, B. B., and Liu, J. W., 2012. Expression and activity analysis of thioredoxin from marine coccolithophorid Emiliania huxleyi in Pichia pastoris. Oceanologia et Limnologia Sinica, 43(5): 905–910.

    Google Scholar 

  • Castberg, T., Thyrhaug, R., Larsen, A., Sandaa, R. A., and Heldal, M. V., 2002. Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). Journal of Phycology, 38(4): 767–774.

    Article  Google Scholar 

  • Chen, F., Suttle, C. A., and Short, S. M., 1996. Genetic diversity in marine algal virus communities as revealed by sequence analysis of DNA polymerase genes. Applied Environment Microbiology, 62: 2869–2874.

    Google Scholar 

  • Conte, M., van der Wal, P., Veldhuis, M., Knappertsbusch, M., Stefels, J., Brownlee, C., van Bleijswijk, J., Westbroek, P., Young, J., Fernandez, E., Brown, C. W., Jordan, R., Egge, J., and Brummer, G. J., 1993. A model system approach to biological climate forcing. The example of Emiliania huxleyi. Global and Planetary Change, 8(1–2): 27–46.

    Google Scholar 

  • Coolen, M. J. L., 2011. 7000 Years of Emiliania huxleyi viruses in the Black Sea. Science, 333(6041): 451–452.

    Article  Google Scholar 

  • Dunigan, D. D., Fitzgerald, L. A., and Van Etten, J. L., 2006. Phycodnaviruses: A peek at genetic diversity. Virus Research, 117(1): 119–132.

    Article  Google Scholar 

  • Forterre, P., and Prangishvili, D., 2009. The origin of viruses. Research in Microbiology, 160(7): 466–472.

    Article  Google Scholar 

  • Frada, M. J., Bidle, K. D., Probert, I., and de Vargas, C., 2012. In situ survey of life cycle phases of the coccolithophore Emiliania huxleyi (Haptophyta). Environmental Microbiology, 14(6): 1558–1569.

    Article  Google Scholar 

  • Frada, M., Probert, I., Allen, M. J., Wilson, W. H., and de Vargas, C., 2008. The ‘Cheshire Cat’ escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proceedings of the National Academy of Sciences of the United States of America, 105(41): 15944–15949.

    Article  Google Scholar 

  • Han, G., Gable, K., Yan, L., Allen, M. J., Wilsonm W. H., Moitra, P., Harmon, J. M., and Dunn, T. M., 2006. Expression of a novel marine viral single chain serine palmitoyltransferase and construction of yeast and mammalian single-chain chimera. Journal of Biology Chemistry, 281: 39935–39942.

    Article  Google Scholar 

  • Hill, R. W., White, B. A., Cottrell, M. T., and Dacey, J. W. H., 1998. Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: A potential climate process. Aquatic Microbial Ecology, 14: 1–6.

    Article  Google Scholar 

  • Holligan, P. M., Viollier, M., Harbour, D. S., Camus, P., and Champagne-Philippe, M., 1983. Satellite and ship studies of coccolithophore production along a continental shelf edge. Nature, 304(5924): 339–342.

    Article  Google Scholar 

  • Kegel, J. U., Blaxter, M., Allen, M. J., Michael, J., Metfies, K., Wilson, W. H., and Valentin, K., 2010. Transcriptional host-virus interaction of Emiliania huxleyi (Haptophyceae) and EhV-86 deduced from combined analysis of expressed sequence tags and microarrays. European Journal of Phycology, 45(1): 1–12.

    Article  Google Scholar 

  • Liu, J. W., Zheng, T. L., Bratbak, G., and Thyrhaug, R., 2011. Virus infection disturbs cyclin expression, leading to cell cycle arrest in the unicellular marine algae Emiliania huxleyi and Chrysochromulina ericina. African Journal of Microbiology Research, 5(14): 1801–1807.

    Google Scholar 

  • Liu, J. W., Zhang, Z. L., Liu, X. H., Cai, Y. Q., and Cai, H. N., 2013. Cloning, expression of the major capsid protein gene from marine algae Emiliania huxleyi virus and the possible use in detection of virus infection. Microbiology Research, 4(1): 21–25.

    Article  Google Scholar 

  • Liu, X. H., Zheng, T. L., Cai, Y. X., and Liu, J. W., 2012. Cloning, expression and characterization of serine palmitoyltransferase (SPT)-like gene subunit (LCB2) from marine Emiliania huxleyi virus (Coccolithovirus). Acta Oceanologica Sinica, 31(6): 127–138.

    Article  Google Scholar 

  • Mackinder, L. C. M., Worthy, C. A., Biggi, G., Hall, M., Ryan, K. P., Varsani, A., Harper, G. M., Wilson, W. H., Brownlee, C., and Schroeder, D. C., 2009. A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. Journal of General Virology, 90(9): 2306–2316.

    Article  Google Scholar 

  • Marsh, M. E., 2003. Regulation of CaCO3 formation in coccolithophores. Comparative Biochemistry Physiology B: Biochemistry Molecular Biology, 136: 743–754.

    Article  Google Scholar 

  • Martínez, J. M., Schroeder, D. C., and Wilson, W. H., 2012. Dynamics and genotypic composition of Emiliania huxleyi and their co-occurring viruses during a coccolithophore bloom in the North Sea. FEMS Microbiology Ecology, 81(2):315–323.

    Article  Google Scholar 

  • Masutani, H., Ueda, S, and Yodoi, J., 2005. The thioredoxin system in retroviral infection and apoptosis. Cell Death and Differentiation, 12(1): 991–998.

    Article  Google Scholar 

  • McDaniel, L. D., Young, E., Delaney, J., Ruhnau, F., Ritchie, K. B., and Paul, J. H., 2010. High frequency of horizontal gene transfer in the oceans. Science, 330(6000): 0036–8075.

    Article  Google Scholar 

  • Monier, A., Pagarete, A., de Vargas, C., Allen, M. J., Read, B., Claverie, J. M., and Ogata, H., 2009. Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Research, 19(8): 1441–1449.

    Article  Google Scholar 

  • Monier, A., Welsh, R. M., Gentemann, C., Weinstock, G., Sodergren, E., Armbrust, E. V., Eisen, J. A., and Worden, A. Z., 2012. Phosphate transporters in marine phytoplankton and their viruses: Cross-domain commonalities in viral-host gene exchanges. Environmental Microbiology, 14(1): 162–176.

    Article  Google Scholar 

  • Nagasaki, K., Shirai, Y., Tomaru, Y., Nishida, K., and Pietrokovski, S., 2005. Algal viruses with distinct intraspecies host specificities include identical intein elements. Applied and Environmental Microbiology, 71: 3599–3607.

    Article  Google Scholar 

  • Nissimov, J. I., Worthy, C. A., Rooks, P., Napier, J. A., Kimmance, S. A., Henn, M. R., Ogata, H., and Allen, M. J., 2011a. Draft genome sequence of the coccolithovirus EhV-84. Standards in Genomic Sciences, 5(1): 1–11.

    Article  Google Scholar 

  • Nissimov, J. I., Worthy, C. A., Rooks, P., Napier, J. A., Kimmance, S. A., Henn, M. R., Ogata, H., and Allen, M. J., 2011b. Draft genome sequence of the coccolithovirus Emiliania huxleyi virus 203. Journal of Virology, 85: 13468–13469.

    Article  Google Scholar 

  • Nissimov, J. I., Worthy, C. A., Rooks, P., Napier, J. A., Kimmance, S. A., Henn, M. R., Ogata, H., and Allen, M. J., 2012a. Draft genome sequence of four coccolithoviruses: Emiliania huxleyi virus EhV-88, EhV-201, EhV-207, and EhV-208. Journal of Virology, 86(5): 2896–2897.

    Article  Google Scholar 

  • Nissimov, J. I., Worthy, C. A., Rooks, P., Napier, J. A., Kimmance, S. A., Henn, M. R., Ogata, H., and Allen, M. J., 2012b. Draft genome sequence of the coccolithovirus Emiliania huxleyi virus 202. Journal of Virology, 86: 2380–2381.

    Article  Google Scholar 

  • Nissimov, J. I., Jones, M., Napier, J. A., Munn, C. B., Kimmance, S. A., and Allen, M. J., 2013. Functional inferences of environmental coccolithovirus biodiversity. Virologica Sinica, 28(5): 291–302.

    Article  Google Scholar 

  • Nissimov, J. I., Napier, J. A., Kimmance, S. A., and Allen, M. J., 2014. Permanent draft genomes of four new coccolithoviruses: EhV-18, EhV-145, EhV-156 and EhV-164. Marine Genomics, 15: 7–8.

    Article  Google Scholar 

  • Pagarete, A., Allen, M. J., Wilson, W. H., Kimmance, S. A., and de Vargas, C., 2009. Host-virus shift of the sphingolipid pathway along an Emiliania huxleyi bloom: Survival of the fattest. Environmental Microbiology, 11(11): 2840–2848.

    Article  Google Scholar 

  • Pagarete, A., Lanzén, A., Puntervoll, P., Sandaa, R. A., Larsen, A., Larsen, J. B., Allen, M. J., and Bratbak, G., 2012. Genomic sequence and analysis of EhV-99B1, a new coccolithovirus from the Norwegian Fjords. Intervirology, 56: 60–66.

    Article  Google Scholar 

  • Rickaby, R. E. M., Bard, E., Sonzogni, C., Rostek, F., Beaufort, L., Barker, S., Rees, G., and Schrag, D. P., 2007. Coccolith chemistry reveals secular variations in the global ocean carbon cycle? Earth and Planet Science Letters, 253(1–2): 83–95.

    Article  Google Scholar 

  • Ridgwell, A., and Zeebe, R. E., 2005. The role of the global carbonate cycle in the regulation and evolution of the Earth system. Earth and Planet Science Letters, 234(3–4): 299–315.

    Article  Google Scholar 

  • Rohwer, F., and Thurber, R. V., 2009. Viruses manipulate the marine environment. Nature, 459(14): 207–212.

    Article  Google Scholar 

  • Rowe, J. M., Fabre, M. F., Gobena, D., Wilson, W. H., and Wilhelm, S. W., 2011. Application of the major capsid protein as a marker of the phylogenetic diversity of Emiliania huxleyi viruses. FEMS Microbiology Ecology, 76: 373–380.

    Article  Google Scholar 

  • Schroeder, D. C., Oke, J., Hall, M., Malin, G., and Wilson, W. H., 2003. Virus succession observed during an Emiliania huxleyi Bloom. Applied and Environmental Microbiology, 69(5): 2484–2490.

    Article  Google Scholar 

  • Schroeder, D. C., Oke, J., Malin, G., and Wilson, W. H., 2002. Coccolithovirus (Phycodnaviridae): Characterisation of a new large dsDNA) algal virus that infects Emiliania huxleyi. Archives of Virology, 147: 1685–1698.

    Article  Google Scholar 

  • Sorensen, G., Baker, A. C., Hall, M. J., Munn, C. B., and Schroeder, D. C., 2009. Novel virus dynamics in an Emiliania huxleyi bloom. Journal of Plankton Research, 31(7): 787–791.

    Article  Google Scholar 

  • Sutterwala, S. S., Creswell, C. H., Sanyal, S., Menon, A. K., and Bangs, J. D., 2007. De novo sphingolipid synthesis is essential for viability, but not for transport of glycosylphosphatidy-linositol-anchored proteins, in African trypanosomes. Eukaryotic Cell, 6(3): 454–464.

    Article  Google Scholar 

  • Suttle, C. A., 2005. Viruses in the sea. Nature, 437: 356–361.

    Article  Google Scholar 

  • Takemura, M., 2002. Poxviruses and the origin of the eukaryotic nucleus. Journal of Molecular Evolution, 52(5): 419–425.

    Google Scholar 

  • Van Etten, J. L., 2011. Another really, really big virus. Viruses, 3(1): 32–46.

    Article  Google Scholar 

  • Vardi, A., Haramaty, L., Van Mooy, B. A. S., Fredricks, H. F., Kimmance, S. A., Larsen, A., and Bidle, K. D., 2012. Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proceedings of the National Academy of Sciences, 109(47): 19327–19332.

    Article  Google Scholar 

  • Vardi, A., Van Mooy, B. A. S., Fredricks, H. F., Popendorf, K. J., Ossolinski, J. E., Haramaty, L., and Bidle, K. D., 2009. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science, 326(5954): 861–865.

    Article  Google Scholar 

  • Vogt, M., Steinke, M., Turner, S., Paulino, A., Meyerhfer, M., Riebesell, U., LeQuéré, C., and Liss, P., 2008. Dynamics of dimethylsulphoniopropionate and dimethylsulphide under different CO2 concentrations during a mesocosm experiment. Biogeosciences Discuss, 5: 407–419.

    Article  Google Scholar 

  • Wilson, W. H., Schroeder, D. C., Allen, M. J., Holden, M. T. G., Parkhill, J., Barrell, B. G., Churcher, C., Hamlin, N., Mungall, K., Norbertczak, H., Quail, M. A., Price, C., Rabbinowitsch, E., Walker, D., Craigon, M., Roy, D., and Ghazal, P., 2005. Complete genome sequence and lyticphase transcription profile of a coccolithovirus. Science, 309: 1090–1092.

    Article  Google Scholar 

  • Wilson, W. H., Tarran, G. A., Schroeder, D., Cox, M., Oke, J., and Malin G., 2002. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. Journal of the Marine Biological Association of the United Kingdom, 82(3): 369–377.

    Article  Google Scholar 

  • Wolfe, G. V., Steinke, M., and Kirst, G. O., 1997. Grazing activated chemical defense in a unicellular marine alga. Nature, 387: 894–897.

    Article  Google Scholar 

  • Zhang, Y. F., Liu, J. W., Zhang, Z. L., and Dong, S. L., 2010. Cloning and bioinformatic analysis of thioredoxin-like protein gene in marine coccolithophorid Emiliania huxleyi virus. Oceanologia et Limnologia Sinica, 40(2): 294–297.

    Google Scholar 

  • Zhaxybayeva, O., and Gogarten, J. P., 2007. Horizontal gene transfer, gene histories, and the root of the tree of life. In: Planetary Systems and the Origins of Life. Cambridge Uiversity Press, UK, 178–192.

    Chapter  Google Scholar 

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Authors and Affiliations

  1. College of Food and Bioengineering, Jimei University, Xiamen, 361021, P. R. China

    Jingwen Liu & Miaomiao Xu

  2. Research Center of Food Microbiology and Enzyme Engineering Technology of Fujian Province, Xiamen, 361021, P. R. China

    Jingwen Liu & Miaomiao Xu

  3. State Key Laboratory for Marine Environmental Sciences and Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystem, School of Life Sciences, Xiamen University, Xiamen, 361005, P. R. China

    Tianling Zheng

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  1. Jingwen Liu
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Correspondence to Tianling Zheng.

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Liu, J., Xu, M. & Zheng, T. A minireview of marine algal virus — Coccolithoviruses. J. Ocean Univ. China 14, 293–300 (2015). https://doi.org/10.1007/s11802-015-2623-z

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