The cosmopolitan calcifying alga Emiliania huxleyi is one of the most abundant bloom forming coccolithophore species in the oceans and plays an important role in global biogeochemical cycling. Coccolithoviruses are a major cause of coccolithophore bloom termination and have been studied in laboratory, mesocosm and open ocean studies. However, little is known about the dynamic interactions between the host and its viruses, and less is known about the natural diversity and role of functionally important genes within natural coccolithovirus communities. Here, we investigate the temporal and spatial distribution of coccolithoviruses by the use of molecular fingerprinting techniques PCR, DGGE and genomic sequencing. The natural biodiversity of the virus genes encoding the major capsid protein (MCP) and serine palmitoyltransferase (SPT) were analysed in samples obtained from the Atlantic Meridional Transect (AMT), the North Sea and the L4 site in the Western Channel Observatory. We discovered nine new coccolithovirus genotypes across the AMT and L4 site, with the majority of MCP sequences observed at the deep chlorophyll maximum layer of the sampled sites on the transect. We also found four new SPT gene variations in the North Sea and at L4. Their translated fragments and the full protein sequence of SPT from laboratory strains EhV-86 and EhV-99B1 were modelled and revealed that the theoretical fold differs among strains. Variation identified in the structural distance between the two domains of the SPT protein may have an impact on the catalytic capabilities of its active site. In summary, the combined use of ‘standard’ markers (i.e. MCP), in combination with metabolically relevant markers (i.e. SPT) are useful in the study of the phylogeny and functional biodiversity of coccolithoviruses, and can provide an interesting intracellular insight into the evolution of these viruses and their ability to infect and replicate within their algal hosts.
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Abrescia N G, Bamford D H, Grimes J M, and Stuart D I. 2012. Structure unifies the viral universe. Annu Rev Biochem, 81: 795–822.
Allen M J, Schroeder D C, Holden M T, and Wilson W H. 2006. Evolutionary History of the Coccolithoviridae. Mol Biol Evol, 23: 86–92.
Allen M J, Schroeder D C, Donkin A, Crawfurd K J, and Wilson W H. 2006. Genome comparison of two Coccolithoviruses. Virol J, 3: 15.
Allen M J, Martinez-Martinez J, Schroeder D C, Somerfield P J, and Wilson W H. 2007. Use of microarrays to assess viral diversity: from genotype to phenotype. Environ Microbiol, 9: 971–982.
Allen M J, Forster T, Schroeder D C, Hall M, Roy D, Ghazal P, and Wilson W H. 2006. Locus-specific gene expression pattern suggests a unique propagation strategy for a giant algal virus. J Virol, 80: 7699–7705.
Bamford D H, Grimes J M, and Stuart D I. 2005. What does structure tell us about virus evolution?. Curr Opin Struct Biol, 15: 655–663.
Bidle K D, and Vardi A. 2011. A chemical arms race at sea mediates algal host-virus interactions. Curr Opin Microbiol, 14: 449–457.
Bidle K D, Haramaty L, Barcelos E R J, and Falkowski P. 2007. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc Natl Acad Sci U S A, 104: 6049–6054.
Brussaard C P, Marie D, and Bratbak G. 2000. Flow cytometric detection of viruses. J Virol Methods, 85: 175–182.
Brussaard C P, Wilhelm S W, Thingstad F, Weinbauer M G, Bratbak G, Heldal M, Kimmance S A, Middelboe M, Nagasaki K, Paul J H, Schroeder D C, Suttle C A, Vaque D, and Wommack K E. 2008. Global-scale processes with a nanoscale drive: the role of marine viruses. ISME J, 2: 575–578.
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. Appl Environ Microbiol, 62: 2869–2874.
Coolen M J. 2011. 7000 years of Emiliania huxleyi viruses in the Black Sea. Science, 333: 451–452.
de Wit R, and Bouvier T. 2006. ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say?. Environ Microbiol, 8: 755–758.
Falkowski P G, Fenchel T, and Delong E F. 2008. The microbial engines that drive Earth’s biogeochemical cycles. Science, 320: 1034–1039.
Guex N, and Peitsch M C. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis, 18: 2714–2723.
Han G, Gable K, Yan L, Allen M J, Wilson 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. J Biol Chem, 281: 39935–39942.
Hanson R. 2010. Jmol — a paradigm shift in crystallographic visualization. Journal of Applied Crystallography, 43: 1250–1260.
Hartshorn M J. 2002. AstexViewer: a visualisation aid for structure-based drug design. J Comput Aided Mol Des, 16: 871–881.
Kelley L A, and Sternberg M J. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc, 4: 363–371.
Krupovic M, and Bamford D H. 2008. Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol, 6: 941–948.
Krupovic M, and Bamford D H. 2011. Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr Opin Virol, 1: 118–124.
Larsen J B, Larsen A, Bratbak G, and Sandaa R A. 2008. Phylogenetic analysis of members of the Phycodnaviridae virus family, using amplified fragments of the major capsid protein gene. Appl Environ Microbiol, 74: 3048–3057.
Martinez 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 Microbiol Ecol, 81: 315–323.
Martinez J M, Schroeder D C, Larsen A, Bratbak G, and Wilson W H. 2007. Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl Environ Microbiol, 73: 554–562.
Michaelson L V, Dunn T M, and Napier J A. 2010. Viral trans-dominant manipulation of algal sphingolipids. Trends Plant Sci, 15: 651–655.
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 Res, 19: 1441–1449.
Nissimov J I, Worthy C A, Rooks P, Napier J A, Kimmance S A, Henn M R, Ogata H, and Allen M J. 2011. Draft genome sequence of the coccolithovirus EhV-84. Stand Genomic Sci, 5: 1–11.
Nissimov J I, Worthy C A, Rooks P, Napier J A, Kimmance S A, Henn M R, Ogata H, and Allen M J. 2011. Draft genome sequence of the Coccolithovirus Emiliania huxleyi virus 203. J Virol, 85: 13468–13469.
Nissimov J I, Worthy C A, Rooks P, Napier J A, Kimmance S A, Henn M R, Ogata H, and Allen M J. 2012. Draft genome sequence of the coccolithovirus Emiliania huxleyi virus 202. J Virol, 86: 2380–2381.
Nissimov J I, Worthy C A, Rooks P, Napier J A, Kimmance S A, Henn M R, Ogata H, and Allen M J. 2012. Draft genome sequence of four coccolithoviruses: Emiliania huxleyi virus EhV-88, EhV-201, EhV-207, and EhV-208. J Virol, 86: 2896–2897.
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. Environ Microbiol, 11: 2840–2848.
Pagarete A, Le Corguille G, Tiwari B, Ogata H, de Vargas C, Wilson W H, and Allen M J. 2011. Unveiling the transcriptional features associated with coccolithovirus infection of natural Emiliania huxleyi blooms. FEMS Microbiol Ecol, 78: 555–564.
Pagarete A, Lanzen 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.
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 Microbiol Ecol, 76: 373–380.
Saitou N, and Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol, 4: 406–425.
Schroeder D C, Oke J, Hall M, Malin G, and Wilson W H. 2003. Virus succession observed during an Emiliania huxleyi bloom. Appl Environ Microbiol, 69: 2484–2490.
Schroeder D C, Biggi G F, Hall M, Davy J, Martínez J M, Richardson A J, Malin G, and Wilson W H. 2005. A GENETIC MARKER TO SEPARATE EMILIANIA HUXLEYI (PRYMNESIOPHYCEAE) MORPHOTYPES1. Journal of Phycology, 41: 874–879.
Suttle C A. 2005. Viruses in the sea. Nature, 437: 356–361.
Suttle C A. 2007. Marine viruses—major players in the global ecosystem. Nat Rev Microbiol, 5: 801–812.
Tamura K, Dudley J, Nei M, and Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol, 24: 1596–1599.
van Rijssel M, and Gieskes W W C. 2002. Temperature, light, and the dimethylsulfoniopropionate (DMSP) content of Emiliania huxleyi (Prymnesiophyceae). Journal of Sea Research, 48: 17–27.
Vardi A, Van Mooy B A, 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: 861–865.
Vardi A, Haramaty L, Van Mooy B A, 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. Proc Natl Acad Sci U S A.
Wilson W H, Tarran G, and Zubkov M V. 2002. Virus dynamics in a coccolithophore-dominated bloom in the North Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 49: 2951–2963.
Wilson W H, Schroeder D C, Allen M J, Holden M T, 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 lytic phase transcription profile of a Coccolithovirus. Science, 309: 1090–1092.
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Nissimov, J.I., Jones, M., Napier, J.A. et al. Functional inferences of environmental coccolithovirus biodiversity. Virol. Sin. 28, 291–302 (2013). https://doi.org/10.1007/s12250-013-3362-1
- Major capsid protein
- Serine palmitoyltransferase
- Functional biodiversity