Science China Life Sciences

, Volume 61, Issue 12, pp 1486–1502 | Cite as

Diversity, evolutionary contribution and ecological roles of aquatic viruses

  • Qi-Ya Zhang
  • Jian-Fang GuiEmail author


Aquatic viruses include infected viruses in aquatic animals, plants and microorganisms, and free-floating viruses (virioplankton) in water environments. In the last three decades, a huge number of aquatic viruses, especially diverse free-floating viruses, including cyanophages, phycoviruses, archaea viruses, giant viruses, and even virophages, have been identified by virological experiments and metagenomic analyses. Based on a comprehensive introduction of aquatic virus classification and their morphological and genetic diversity, here, we summarize and outline main virus species, their evolutionary contribution to aquatic communities through horizontal gene transfer, and their ecological roles for cyanobacterial bloom termination and global biogeochemical cycling in freshwater and marine ecosystems. Thereby, some novel insights of aquatic viruses and virus-host interactions, especially their evolutionary contribution and ecological rolesin diverse aquatic communities and ecosystems, are highlighted in this review.


aquatic virus diversity virus-host interaction horizontal gene transfer evolutionary contribution aquatic ecosystem biogeochemical cycling 


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This work was supported by grants from the National Natural Science Foundation of China (31430091, 31772890) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA08030202).


  1. Abergel, C., Legendre, M., and Claverie, J.M. (2015). The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. FEMS MicroBiol Rev 39, 779–796.Google Scholar
  2. Abrahão, J., Silva, L., Silva, L.S., Khalil, J.Y.B., Rodrigues, R., Arantes, T., Assis, F., Boratto, P., Andrade, M., Kroon, E.G., et al. (2018). Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat Commun 9, 749.Google Scholar
  3. Adel, M., Elbehery, A.H.A., Aziz, S.K., Aziz, R.K., Grossart, H.P., and Siam, R. (2016). Viruses-to-mobile genetic elements skew in the deep Atlantis II brine pool sediments. Sci Rep 6, 32704.Google Scholar
  4. Adriaenssens, E.M., Edwards, R., Nash, J.H.E., Mahadevan, P., Seto, D., Ackermann, H.W., Lavigne, R., and Kropinski, A.M. (2015). Integration of genomic and proteomic analyses in the classification of the Siphoviridae family. Virology 477, 144–154.Google Scholar
  5. Adriaenssens, E.M., Wittmann, J., Kuhn, J.H., Turner, D., Sullivan, M.B., Dutilh, B.E., Jang, H.B., van Zyl, L.J., Klumpp, J., Lobocka, M., et al. (2018). Taxonomy of prokaryotic viruses: 2017 update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol 163, 1125–1129.Google Scholar
  6. Aguirre de Cárcer, D., López-Bueno, A., Pearce, D.A., and Alcamí, A. (2015). Biodiversity and distribution of polar freshwater DNA viruses. Sci Adv 1, e1400127.Google Scholar
  7. 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 Virology 80, 7699–7705.Google Scholar
  8. Altermann, W., Kazmierczak, J., Oren, A., and Wright, D.T. (2006). Cyanobacterial calcification and its rock-building potential during 3.5 billion years of Earth history. Geobiology 4, 147–166.Google Scholar
  9. Andam, C.P., Carver, S.M., and Berthrong, S.T. (2015). Horizontal gene flow in managed ecosystems. Annu Rev Ecol Evol Syst 46, 121–143.Google Scholar
  10. Ankrah, N.Y.D., May, A.L., Middleton, J.L., Jones, D.R., Hadden, M.K., Gooding, J.R., LeCleir, G.R., Wilhelm, S.W., Campagna, S.R., and Buchan, A. (2014). Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J 8, 1089–1100.Google Scholar
  11. Arnold, H.P., Ziese, U., and Zillig, W. (2000). SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 272, 409–416.Google Scholar
  12. Arslan, D., Legendre, M., Seltzer, V., Abergel, C., and Claverie, J.M. (2011). Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA 108, 17486–17491.Google Scholar
  13. Avarre, J.C. (2017). Editorial: molecular tracing of aquatic viruses: where epidemiology needs to meet genomics. Front Microbiol 8, 1498.Google Scholar
  14. Avrani, S., Schwartz, D.A., and Lindell, D. (2012). Virus-host swinging party in the oceans. Mobile Genet Elem 2, 88–95.Google Scholar
  15. Bamford, D.H., Pietilä, M.K., Roine, E., Atanasova, N.S., Dienstbier, A., Oksanen, H.M., and Ictv Report Consortium, H.M. (2017). ICTV virus taxonomy profile: Pleolipoviridae. J General Virology 98, 2916–2917.Google Scholar
  16. Beckett, S.J., and Williams, H.T.P. (2013). Coevolutionary diversification creates nested-modular structure in phage-bacteria interaction networks. Interface Focus 3, 20130033.Google Scholar
  17. Bellec, L., Grimsley, N., Moreau, H., and Desdevises, Y. (2009). Phylogenetic analysis of new Prasinoviruses (Phycodnaviridae) that infect the green unicellular algae Ostreococcus, Bathycoccus and Micromonas. Environ MicroBiol Rep 1, 114–123.Google Scholar
  18. Beraldi-Campesi, H. (2013). Early life on land and the first terrestrial ecosystems. Ecol Process 2, 1.Google Scholar
  19. Bettstetter, M., Peng, X., Garrett, R.A., and Prangishvili, D. (2003). AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus. Virology 315, 68–79.Google Scholar
  20. Berliner, A.J., Mochizuki, T., and Stedman, K.M. (2018). Astrovirology: viruses at large in the universe. Astrobiology 18, 207–223.Google Scholar
  21. Boyer, M., Azza, S., Barrassi, L., Klose, T., Campocasso, A., Pagnier, I., Fournous, G., Borg, A., Robert, C., Zhang, X., et al. (2011). Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci USA 108, 10296–10301.Google Scholar
  22. Breitbart, M., and Rohwer, F. (2005). Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13, 278–284.Google Scholar
  23. Breitbart, M., Bonnain, C., Malki, K., and Sawaya, N.A. (2018). Phage puppet masters of the marine microbial realm. Nat Microbiol 3, 754–766.Google Scholar
  24. Breitbart, M., Thompson, L., Suttle, C., and Sullivan, M. (2007). Exploring the vast diversity of marine viruses. Oceanography 20, 135–139.Google Scholar
  25. Breitbart, M. (2012). Marine viruses: Truth or dare. Annu Rev Mar Sci 4, 425–448.Google Scholar
  26. Buchan, A., LeCleir, G.R., Gulvik, C.A., and González, J.M. (2014). Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Micro 12, 686–698.Google Scholar
  27. Cavicchioli, R., and Erdmann, S. (2015). The discovery of Antarctic RNA viruses: a new game changer. Mol Ecol 24, 4809–4811.Google Scholar
  28. Cheraw, J.E.Jr., Tyson, J., Bedwell, G.J., Brooke, D., Edwards, A.G., Dokland, T., Prevelige, P.E., and Fane, B.A. (2017). ?X174 procapsid assembly: effects of an inhibitory external scaffolding protein and resistant coat proteins in vitro. J Virol 91, e01878–16.Google Scholar
  29. Chinchar, V.G., Hick, P., Ince, I.A., Jancovich, J.K., Marschang, R., Qin, Q. W., Subramaniam, K., Waltzek, T.B., Whittington, R., Williams, T., and Zhang, Q.Y. (2017). ICTV virus taxonomy profile: iridoviridae. J Gen Virol 98, 890–891.Google Scholar
  30. Claverie, J.M. (2006). Viruses take center stage in cellular evolution.. Genome Biol 7, 110.Google Scholar
  31. Claverie, J.M., and Abergel, C. (2009). Mimivirus and its virophage. Annu Rev Genet 43, 49–66.Google Scholar
  32. Claverie, J.M., Abergel, C., and Ogata, H. (2009). Mimivirus. Curr Top Microbiol Immunol 328, 89–121.Google Scholar
  33. Claverie, J.M., and Abergel, C. (2010). Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genets 26, 431–437.Google Scholar
  34. Colombo, S., Arioli, S., Guglielmetti, S., Lunelli, F., and Mora, D. (2016). Virome-associated antibiotic-resistance genes in an experimental aquaculture facility. FEMS MicroBiol Ecol 92, fiw003–5.Google Scholar
  35. Colombo, S., Arioli, S., Neri, E., Della Scala, G., Gargari, G., and Mora, D. (2017). Viromes as genetic reservoir for the microbial communities in aquatic environments: a focus on antimicrobial-resistance genes. Front Microbiol 8, 1095.Google Scholar
  36. Colson, P., Pagnier, I., Yoosuf, N., Fournous, G., La Scola, B., and Raoult, D. (2013). “Marseilleviridae”, a new family of giant viruses infecting amoebae. Arch Virol 158, 915–920.Google Scholar
  37. Colson, P., Yutin, N., Shabalina, S.A., Robert, C., Fournous, G., La Scola, B., Raoult, D., and Koonin, E.V. (2011). Viruses with more than 1,000 genes: mamavirus, a new acanthamoeba polyphagamimivirus strain, and reannotation of mimivirus genes. Genome Biol Evol 3, 737–742.Google Scholar
  38. Culley, A.I., Lang, A.S., and Suttle, C.A. (2006). Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–1798.Google Scholar
  39. Culley, A.I., Mueller, J.A., Belcaid, M., Wood-Charlson, E.M., Poisson, G., and Steward, G.F. (2014). The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. mBio 5, e01210–14.Google Scholar
  40. Danovaro, R., Dell’Anno, A., Corinaldesi, C., Magagnini, M., Noble, R., Tamburini, C., and Weinbauer, M. (2008). Major viral impact on the functioning of benthic deep-sea ecosystems. Nature 454, 1084–1087.Google Scholar
  41. Davín, A.A., Tannier, E., Williams, T.A., Boussau, B., Daubin,V., and Szöllosi, G.J. (2018). Gene transfers can date the tree of life. Nat Ecol Evol 2, 904–909.Google Scholar
  42. Delaroque, N., and Boland, W. (2008). The genome of the brown alga Ectocarpus siliculosus contains a series of viral DNA pieces, suggesting an ancient association with large dsDNA viruses. BMC Evol Biol 8, 110.Google Scholar
  43. Deng, L., Ignacio-Espinoza, J.C., Gregory, A.C., Poulos, B.T., Weitz, J.S., Hugenholtz, P., and Sullivan, M.B. (2014). Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513, 242–245.Google Scholar
  44. Desnues, C., La Scola, B., Yutin, N., Fournous, G., Robert, C., Azza, S., Jardot, P., Monteil, S., Campocasso, A., Koonin, E.V., et al. (2012). Provirophages and transpovirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci USA 109, 18078–18083.Google Scholar
  45. Díaz-Muñoz, S.L., Tenaillon, O., Goldhill, D., Brao, K., Turner, P.E., and Chao, L. (2013). Electrophoretic mobility confirms reassortment bias among geographic isolates of segmented RNA phages. BMC Evol Biol 13, 206.Google Scholar
  46. DiMaio, F., Yu, X., Rensen, E., Krupovic, M., Prangishvili, D., and Egelman, E.H. (2015). A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348, 914–917.Google Scholar
  47. Dornas, F.P., Assis, F.L., Aherfi, S., Arantes, T., Abrahão, J.S., Colson, P., and La Scola, B. (2016). A Brazilian marseillevirus is the founding member of a lineage in family Marseilleviridae. Viruses 8, 76.Google Scholar
  48. Dunlap, D.S., Ng, T.F.F., Rosario, K., Barbosa, J.G., Greco, A.M., Breitbart, M., and Hewson, I. (2013). Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci USA 110, 1375–1380.Google Scholar
  49. Edwards, R.A., and Rohwer, F. (2005). Viral metagenomics. Nat Rev Micro 3, 504–510.Google Scholar
  50. Feiner, R., Argov, T., Rabinovich, L., Sigal, N., Borovok, I., and Herskovits, A.A. (2015). A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Micro 13, 641–650.Google Scholar
  51. Filée, J., Siguier, P., and Chandler, M. (2007). I am what I eat and I eat what I am: Acquisition of bacterial genes by giant viruses. Trends Genets 23, 10–15.Google Scholar
  52. Filée, J. (2015). Genomic comparison of closely related Giant Viruses supports an accordion-like model of evolution. Front Microbiol 6, 593.Google Scholar
  53. Finke, J.F., Winget, D.M., Chan, A.M., and Suttle, C.A. (2017). Variation in the genetic repertoire of viruses infecting Micromonas pusilla reflects horizontal gene transfer and links to their environmental distribution. Viruses 9, 116.Google Scholar
  54. Fischer, M.G., Allen, M.J., Wilson, W.H., and Suttle, C.A. (2010). Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 107, 19508–19513.Google Scholar
  55. Forterre, P., Krupovic, M., and Prangishvili, D. (2014). Cellular domains and viral lineages. Trends Micro Biol 22, 554–558.Google Scholar
  56. Frost, L.S., Leplae, R., Summers, A.O., and Toussaint, A. (2005). Mobile genetic elements: the agents of open source evolution. Nat Rev Micro 3, 722–732.Google Scholar
  57. Fuhrman, J.A. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548.Google Scholar
  58. Gao, E.B., Gui, J.F., and Zhang, Q.Y. (2012). A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome. J Virology 86, 236–245.Google Scholar
  59. Gao, E., Yuan, X., Li, R., and Zhang, Q. (2009). Isolation of a novel cyanophage infectious to the filamentous cyanobacterium Planktothrix agardhii (Cyanophyceae) from Lake Donghu, China. Aquat Microb Ecol 54, 163–170.Google Scholar
  60. Garcia-Heredia, I., Martin-Cuadrado, A.B., Mojica, F.J.M., Santos, F., Mira, A., Antón, J., and Rodriguez-Valera, F. (2012). Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS ONE 7, e33802.Google Scholar
  61. Gómez, P., and Buckling, A. (2011). Bacteria-phage antagonistic coevolution in soil. Science 332, 106–109.Google Scholar
  62. Goulet, A., Blangy, S., Redder, P., Prangishvili, D., Felisberto-Rodrigues, C., Forterre, P., Campanacci, V., and Cambillau, C. (2009). Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage. Proc Natl Acad Sci USA 106, 21155–21160.Google Scholar
  63. Griffin, D.W. (2013). The quest for extraterrestrial life: what about the viruses? Astrobiology 13, 774–783.Google Scholar
  64. Gui, L., Chinchar, V.G., and Zhang, Q. (2018). Molecular basis of pathogenesis of emerging viruses infecting aquatic animals. Aquaculture Fisheries 3, 1–5.Google Scholar
  65. Gui, L., and Zhang, Q.Y. (2018). Disease prevention and control. In Aquaculture in China: Success Stories and Modern Trends. Gui, J.F., Tang, Q.S., Li, Z.J., Liu, J.S., and Sena, S.S.De. ed. (Chichester, UK, Wiley-Blackwell), pp577–598.Google Scholar
  66. Häring, M., Peng, X., Brügger, K., Rachel, R., Stetter, K.O., Garrett, R.A., and Prangishvili, D. (2004). Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 323, 233–242.Google Scholar
  67. Häring, M., Rachel, R., Peng, X., Garrett, R.A., and Prangishvili, D. (2005). Viral diversity in hot springs of Pozzuoli, Italy, and characterization of a unique archaeal virus, Acidianus bottle-shaped virus, from a new family, the Ampullaviridae. J Virology 79, 9904–9911.Google Scholar
  68. Häring, M., Vestergaard, G., Rachel, R., Chen, L., Garrett, R.A., and Prangishvili, D. (2005). Independent virus development outside a host. Nature 436, 1101–1102.Google Scholar
  69. Hugenholtz, P., and Tyson, G.W. (2008). Metagenomics. Nature 455, 481–483.Google Scholar
  70. Hughes, A.L., and Friedman, R. (2005). Poxvirus genome evolution by gene gain and loss. Mol PhyloGenets Evol 35, 186–195.Google Scholar
  71. Hurwitz, B.L., Hallam, S.J., and Sullivan, M.B. (2013). Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biol 14, R123.Google Scholar
  72. Hurwitz, B.L., and U’Ren, J.M. (2016). Viral metabolic reprogramming in marine ecosystems. Curr Opin MicroBiol 31, 161–168.Google Scholar
  73. Ignacio-Espinoza, J.C., and Sullivan, M.B. (2012). Phylogenomics of T4 cyanophages: Lateral gene transfer in the ‘core’ and origins of host genes. Environ MicroBiol 14, 2113–2126.Google Scholar
  74. James, L., and Van, Etten. (2009). Lesser known large dsDNA viruses. Curr Top Microbiol Immunol 328, (Springer-Verlag Berlin Heidelberg), pp. 1–42.Google Scholar
  75. Jancovich, J.K., Bremont, M., Touchman, J.W., and Jacobs, B.L. (2010). Evidence for multiple recent host species shifts among the Ranaviruses (family Iridoviridae). J Virology 84, 2636–2647.Google Scholar
  76. Jancovich, J.K., Qin, Q., Zhang, Q.Y., and Chinchar, V.G. (2015). Ranavirus replication: molecular, cellular, and immunological events. In Ranaviruses Lethal Pathogens of Ectothermic Vertebrates. Gray, M.J., Chinchar, V.G., ed. (Springer, New York, USA), pp 105–139.Google Scholar
  77. Jover, L.F., Effler, T.C., Buchan, A., Wilhelm, S.W., and Weitz, J.S. (2014). The elemental composition of virus particles: Implications for marine biogeochemical cycles. Nat Rev Micro 12, 519–528.Google Scholar
  78. Kalatzis, P.G., Rørbo, N.I., Castillo, D., Mauritzen, J.J., Jørgensen, J., Kokkari, C., Zhang, F., Katharios, P., and Middelboe, M. (2017). Stumbling across the same phage: comparative genomics of widespread temperate phages infecting the fish pathogen Vibrio anguillarum. Viruses 9, 122.Google Scholar
  79. Keen, E.C., Bliskovsky, V.V., Malagon, F., Baker, J.D., Prince, J.S., Klaus, J.S., and Adhya, S.L. (2017). Novel “superspreader” bacteriophages promote horizontal gene transfer by transformation. mBio 8, e02115–16.Google Scholar
  80. Key, T., Read, J., Nibert, M.L., and Duncan, R. (2013). Piscine reovirus encodes a cytotoxic, non-fusogenic, integral membrane protein and previously unrecognized virion outer-capsid proteins. J General Virology 94, 1039–1050.Google Scholar
  81. King, A.M.Q., Lefkowitz, E., Adams, M.J., and Carstens, E.B. (2012). Virus Taxonomy Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. (Elsevier. San Diego, CA 92101–4495, USA), pp 109–110.Google Scholar
  82. Knowles, B., Silveira, C.B., Bailey, B.A., Barott, K., Cantu, V.A., Cobián- Güemes, A.G., Coutinho, F.H., Dinsdale, E.A., Felts, B., Furby, K.A., et al. (2016). Lytic to temperate switching of viral communities. Nature 531, 466–470.Google Scholar
  83. Koonin, E.V. (2016). Viruses and mobile elements as drivers of evolutionary transitions. Phil Trans R Soc B 371, 20150442.Google Scholar
  84. Koonin, E.V., and Wolf, Y.I. (2008). Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36, 6688–6719.Google Scholar
  85. Krupovic, M., Cvirkaite-Krupovic, V., Iranzo, J., Prangishvili, D., and Koonin, E.V. (2018). Viruses of archaea: structural, functional, environmental and evolutionary genomics. Virus Res 244, 181–193.Google Scholar
  86. Krupovic, M., Prangishvili, D., Hendrix, R.W., and Bamford, D.H. (2011). Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol Mol Biol Rev 75, 610–635.Google Scholar
  87. La Scola, B., Audic, S., Robert, C., Jungang, L., de Lamballerie, X., Drancourt, M., Birtles, R., Claverie, J.M., and Raoult, D. (2003). A giant virus in amoebae. Science 299, 2033.Google Scholar
  88. La Scola, B., de Lamballerie, X.N., Claverie, J.M., Drancourt, M., and Raoult, D. (2005). Genus Mimivirus in Virus Taxonomy. In Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses. Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U., and Ball, L. A. ed, (Elsevier, San Diego, Calif, USA), pp 275–276.Google Scholar
  89. La Scola, B., Desnues, C., Pagnier, I., Robert, C., Barrassi, L., Fournous, G., Merchat, M., Suzan-Monti, M., Forterre, P., Koonin, E., and Raoult, D. (2008). The virophage as a unique parasite of the giant mimivirus. Nature 455, 100–104.Google Scholar
  90. Laber, C.P., Hunter, J.E., Carvalho, F., Collins, J.R., Hunter, E.J., Schieler, B.M., Boss, E., More, K., Frada, M., Thamatrakoln, K., et al. (2018). Coccolithovirus facilitation of carbon export in the North Atlantic. Nat Microbiol 3, 537–547.Google Scholar
  91. Labrie, S.J., Frois-Moniz, K., Osburne, M.S., Kelly, L., Roggensack, S.E., Sullivan, M.B., Gearin, G., Zeng, Q., Fitzgerald, M., Henn, M.R., et al. (2013). Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ MicroBiol 15, 1356–1376.Google Scholar
  92. Legendre, M., Bartoli, J., Shmakova, L., Jeudy, S., Labadie, K., Adrait, A., Lescot, M., Poirot, O., Bertaux, L., Bruley, C., et al. (2014). Thirtythousand- year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci USA 111, 4274–4279.Google Scholar
  93. Legendre, M., Santini, S., Rico, A., Abergel, C., and Claverie, J.M. (2011). Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J 8, 99.Google Scholar
  94. Lennon, J.T., and Martiny, J.B.H. (2008). Rapid evolution buffers ecosystem impacts of viruses in a microbial food web. Ecol Lett 11, 1178–1188.Google Scholar
  95. Leslie, M. (2017). Cell-like giant viruses found. Science 356, 15–16.Google Scholar
  96. Li, S., Ou, T., and Zhang, Q. (2013). Two virus-like particles that cause lytic infections in freshwater cyanobacteria. Virol Sin 28, 303–305.Google Scholar
  97. Liao, X.Y., Ou, T., Gao, H., Xu, X.D., Zhu, R., Zhang, Q.Y. (2014). Main reason for concentric rings plaque formation of virus infecting cyanobacteria (A-4L) in lawns of Anabaena variabilis. Acta Microbiol Sin 54, 191–199. (Chinese with English abstract).Google Scholar
  98. Lindell, D., Sullivan, M.B., Johnson, Z.I., Tolonen, A.C., Rohwer, F., and Chisholm, S.W. (2004). Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101, 11013–11018.Google Scholar
  99. Lindell, D., Jaffe, J.D., Johnson, Z.I., Church, G.M., and Chisholm, S.W. (2005). Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89.Google Scholar
  100. Lindell, D., Jaffe, J.D., Coleman, M.L., Futschik, M.E., Axmann, I.M., Rector, T., Kettler, G., Sullivan, M.B., Steen, R., Hess, W.R., et al. (2007). Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86.Google Scholar
  101. Liu, Y., Ishino, S., Ishino, Y., Pehau-Arnaudet, G., Krupovic, M., and Prangishvili. D. (2017). A novel type of polyhedral viruses infecting hyperthermophilic archaea. J Virol 91, e00589–e00517.Google Scholar
  102. Liu, Y.M., Yuan, X.P., and Zhang, Q.Y. (2006a). Spatial distribution and morphologic diversity of virioplankton in Lake Donghu, China. Acta Oecol 29, 328–334.Google Scholar
  103. Liu, Y.M., Zhang, Q.Y., Yuan, X.P., Li, Z.Q., and Gui, J.F. (2006b). Seasonal variation of virioplankton in a eutrophic shallow lake. Hydrobiologia 560, 323–334.Google Scholar
  104. Lohr, J.E., Chen, F., and Hill, R.T. (2005). Genomic analysis of bacteriophage JL001: insights into its interaction with a spongeassociated alpha-proteobacterium. Appl Environ MicroBiol 71, 1598–1609.Google Scholar
  105. López-Bueno, A., Tamames, J., Velázquez, D., Moya, A., Quesada, A., and Alcamí, A. (2009). High diversity of the viral community from an Antarctic lake. Science 326, 858–861.Google Scholar
  106. López-Bueno, A., Rastrojo, A., Peiró, R., Arenas, M., and Alcamí, A. (2015). Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Mol Ecol 24, 4812–4825.Google Scholar
  107. Mahy, B.W.J., and Van Regenmortel, M.H.V., (2008). Encyclopedia of Virology (2rd edit. Elsevier: Oxford, UK), pp159, 168–170.Google Scholar
  108. Mann, N.H., Clokie, M.R.J., Millard, A., Cook, A., Wilson, W.H., Wheatley, P.J., Letarov, A., and Krisch, H.M. (2005). The genome of S-PM2, a “photosynthetic” T4-type bacteriophage that infects marine synechococcus strains. J Bacteriology 187, 3188–3200.Google Scholar
  109. Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. (2003). Bacterial photosynthesis genes in a virus. Nature 424, 741.Google Scholar
  110. Malik, S.S., Azem-E-Zahra, S., Kim, K.M., Caetano-Anollés, G., and Nasir, A. (2017). Do viruses exchange genes across superkingdoms of Life? Front Microbiol 8, 2110.Google Scholar
  111. Männistö, R.H., Kivelä, H.M., Paulin, L., Bamford, D.H., and Bamford, J. K.H. (1999). The complete genome sequence of PM2, the first lipidcontaining bacterial virus to be isolated. Virology 262, 355–363.Google Scholar
  112. Marie, V., and Lin, J. (2016). Cannibalistic viruses in the aquatic environment: role of virophages in manipulating microbial communities. Int J Environ Sci Technol 13, 2097–2104.Google Scholar
  113. Martínez-Martínez, J., Swan, B.K., and Wilson, W.H. (2014). Marine viruses, a genetic reservoir revealed by targeted viromics. ISME J 8, 1079–1088.Google Scholar
  114. Marston, M.F., Pierciey Jr., F.J., Shepard, A., Gearin, G., Qi, J., Yandava, C., Schuster, S.C., Henn, M.R., and Martiny, J.B.H. (2012). Rapid diversification of coevolving marine Synechococcus and a virus. Proc Natl Acad Sci USA 109, 4544–4549.Google Scholar
  115. Maurice, C.F., Bouvier, C., de Wit, R., and Bouvier, T. (2013). Linking the lytic and lysogenic bacteriophage cycles to environmental conditions, host physiology and their variability in coastal lagoons. Environ Microbiol 15, 2463–2475.Google Scholar
  116. Metzger, M.J., Paynter, A.N., Siddall, M.E., and Goff, S.P. (2018). Horizontal transfer of retrotransposons between bivalves and other aquatic species of multiple phyla. Proc Natl Acad Sci USA 115, E4227–E4235.Google Scholar
  117. Middelboe, M., and Brussaard, C.P.D. (2017). Marine viruses: key players in marine ecosystems. Viruses 9, 302.Google Scholar
  118. Middelboe, M., Jacquet, S., and Weinbauer, M. (2008). Viruses in freshwater ecosystems: an introduction to the exploration of viruses in new aquatic habitats. Freshwater Biol 53, 1069–1075.Google Scholar
  119. Millard, A.D., Zwirglmaier, K., Downey, M.J., Mann, N.H., and Scanlan, D.J. (2009). Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence ofSynechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 11, 2370–2387.Google Scholar
  120. Mizuno, C.M., Rodriguez-Valera, F., Garcia-Heredia, I., Martin-Cuadrado, A.B., and Ghai, R. (2013). Reconstruction of novel cyanobacterial siphovirus genomes from Mediterranean metagenomic fosmids. Appl Environ Microbiol 79, 688–695.Google Scholar
  121. Mochizuki, T., Krupovic, M., Pehau-Arnaudet, G., Sako, Y., Forterre, P., and Prangishvili, D. (2012). Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc Natl Acad Sci USA 109, 13386–13391.Google Scholar
  122. Mochizuki, T., Sako, Y., and Prangishvili, D. (2011). Provirus induction in hyperthermophilic archaea: characterization of Aeropyrum pernix spindle-shaped virus 1 and Aeropyrum pernix ovoid virus 1. J Bacteriology 193, 5412–5419.Google Scholar
  123. Mochizuki, T., Yoshida, T., Tanaka, R., Forterre, P., Sako, Y., and Prangishvili, D. (2010). Diversity of viruses of the hyperthermophilic archaeal genus Aeropyrum, and isolation of the Aeropyrumpernix bacilliform virus 1, APBV1, the first representative of the family Clavaviridae. Virology 402, 347–354.Google Scholar
  124. Monier, A., Larsen, J.B., Sandaa, R.A., Bratbak, G., Claverie, J.M., and Ogata, H. (2008). Marine mimivirus relatives are probably large algal viruses. Virol J 5, 12.Google Scholar
  125. 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.Google Scholar
  126. Moreira, D., and Brochier-Armanet, C. (2008). Giant viruses, giant chimeras: the multiple evolutionary histories of mimivirus genes. BMC Evol Biol 8, 12.Google Scholar
  127. Moreira, D., and López-García, P. (2009). Ten reasons to exclude viruses from the tree of life. Nat Rev Micro 7, 306–311.Google Scholar
  128. Mostajir, B., Amblard, C., Buffan-Dubau, E., De Wit, R., Lensi, R., and Sime-Ngando, T. (2015). Microbial food webs in aquatic and terrestrial Ecosystems. In Environmental Microbiology: Fundamentals and Applications. Bertrand, J.C., Caumette, P., Lebaron, P., Matheron, R., Normand, P., and Sime-Ngando, T. ed. (Springer, the Netherlands), pp 485–509.Google Scholar
  129. Munn, C. (2011). Marine Microbiology: Ecology and Applications, 2nd ed. chapter 1 Microbes in the marine environment. (Garland Science, New York), pp1–23.Google Scholar
  130. Munang’andu, H.M., Mugimba, K.K., Byarugaba, D.K., Mutoloki, S., and Evensen, Ø. (2017). Current advances on virus discovery and diagnostic role of viral metagenomics in aquatic organisms. Front Microbiol 8, 406.Google Scholar
  131. Nagasaki, K. (2008). Dinoflagellates, diatoms, and their viruses. J Microbiol 46, 235–243.Google Scholar
  132. Ogata, H., and Claverie, J.M. (2007). Unique genes in giant viruses: regular substitution pattern and anomalously short size. Genome Res 17, 1353–1361.Google Scholar
  133. Ortmann, A.C., Wiedenheft, B., Douglas, T., and Young, M. (2006). Hot crenarchaeal viruses reveal deep evolutionary connections. Nat Rev Micro 4, 520–528.Google Scholar
  134. Otawa, K., Lee, S.H., Yamazoe, A., Onuki, M., Satoh, H., and Mino, T. (2007). Abundance, diversity, and dynamics of viruses on microorganisms in activated sludge processes. Microb Ecol 53, 143–152.Google Scholar
  135. Ou, T., Li, S., Liao, X., and Zhang, Q. (2013). Cultivation and characterization of the MaMV-DC cyanophage that infects bloomforming cyanobacterium Microcystis aeruginosa. Virol Sin 28, 266–271.Google Scholar
  136. Ou, T., Gao, X.C., Li, S.H., and Zhang, Q.Y. (2015a). Genome analysis and gene nblA identification of Microcystis aeruginosa myovirus (MaMVDC) reveal the evidence for horizontal gene transfer events between cyanomyovirus and host. J General Virology 37, 3681–3697.Google Scholar
  137. Ou, T., Liao, X.Y., Gao, X.C., Xu, X.D., and Zhang, Q.Y. (2015b). Unraveling the genome structure of cyanobacterial podovirus A-4L with long direct terminal repeats. Virus Res 203, 4–9.Google Scholar
  138. Paerl, H.W., and Otten, T.G. (2013). Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65, 995–1010.Google Scholar
  139. Paez-Espino, D., Eloe-Fadrosh, E.A., Pavlopoulos, G.A., Thomas, A.D., Huntemann, M., Mikhailova, N., Rubin, E., Ivanova, N.N., and Kyrpides, N.C. (2016). Uncovering earth’s virome. Nature 536, 425–430.Google Scholar
  140. Palenik, B., Brahamsha, B., Larimer, F.W., Land, M., Hauser, L., Chain, P., Lamerdin, J., Regala, W., Allen, E.E., McCarren, J., et al. (2003). The genome of a motile marine Synechococcus. Nature 424, 1037–1042.Google Scholar
  141. Parada, V., Sintes, E., van Aken, H.M., Weinbauer, M.G., and Herndl, G.J. (2007). Viral abundance, decay, and diversity in the meso- and bathypelagic waters of the North Atlantic. Appl Environ MicroBiol 73, 4429–4438.Google Scholar
  142. Pawlowski, A., Rissanen, I., Bamford, J.K.H., Krupovic, M., and Jalasvuori, M. (2014). Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae. Arch Virol 159, 1541–1554.Google Scholar
  143. Payet, J.P., and Suttle, C.A. (2013). To kill or not to kill: the balance between lytic and lysogenic viral infection is driven by trophic status. Limnol Oceanogr 58, 465–474.Google Scholar
  144. Pearson, H. (2008). ‘Virophage’ suggests viruses are alive. Nature 454, 677.Google Scholar
  145. Pedulla, M.L., Ford, M.E., Houtz, J.M., Karthikeyan, T., Wadsworth, C., Lewis, J.A., Jacobs-Sera, D., Falbo, J., Gross, J., Pannunzio, N.R., et al. (2003). Origins of highly mosaic mycobacteriophage genomes. Cell 113, 171–182.Google Scholar
  146. Peduzzi, P. (2016). Virus ecology of fluvial systems: a blank spot on the map? Biol Rev 91, 937–949.Google Scholar
  147. Peduzzi, P., Gruber, M., Gruber, M., and Schagerl, M. (2014). The virus’s tooth: cyanophages affect an African flamingo population in a bottomup cascade. ISME J 8, 1346–1351.Google Scholar
  148. Pei, C., Lei, X.Y., Yuan, X.P., Wang, D., Zhao, Q.Z., and Zhang, Q.Y. (2012). Herpes-like virus infection in Yangtze finless porpoise (Neophocaena phocaenoides): Pathology, ultrastructure and molecular analysis. J Wildlife Dis 48, 235–237.Google Scholar
  149. Pennisi, E. (2013). Ever-bigger viruses shake tree of life. Science 341, 226–227.Google Scholar
  150. Peng, X., Basta, T., Häring, M., Garrett, R.A., and Prangishvili, D. (2007). Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms. Virology 364, 237–243.Google Scholar
  151. Peng, X., Blum, H., She, Q., Mallok, S., Brügger, K., Garrett, R.A., Zillig, W., and Prangishvili, D. (2001). Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 291, 226–234.Google Scholar
  152. Philippe, N., Legendre, M., Doutre, G., Couté, Y., Poirot, O., Lescot, M., Arslan, D., Seltzer, V., Bertaux, L., Bruley, C., et al. (2013). Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281–286.Google Scholar
  153. Pietilä, M.K., Roine, E., Paulin, L., Kalkkinen, N., and Bamford, D.H. (2009). An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Mol MicroBiol 72, 307–319.Google Scholar
  154. Pietilä, M.K., Roine, E., Sencilo, A., Bamford, D.H., and Oksanen, H.M. (2016). Pleolipoviridae, a newly proposed family comprising archaeal pleomorphic viruses with single-stranded or double-stranded DNA genomes. Arch Virol 161, 249–256.Google Scholar
  155. Pietilä, M.K., Laurinmäki, P., Russell, D.A., Ko, C.C., Jacobs-Sera, D., Butcher, S.J., Bamford, D.H., and Hendrix, R.W. (2013). Insights into head-tailed viruses infecting extremely halophilic archaea. J Virology 87, 3248–3260.Google Scholar
  156. Plumb, J.A., and Hanson, L.A. ed. (2011). Health Maintenance and Principal Microbial Diseases of Cultured Fishes. (Wiley-Blackwell Oxford, UK), pp227–272.Google Scholar
  157. Porter, K., Kukkaro, P., Bamford, J.K.H., Bath, C., Kivelä, H.M., Dyall- Smith, M.L., and Bamford, D.H. (2005). SH1: A novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 335, 22–33.Google Scholar
  158. Prangishvili, D., Arnold, H.P., Götz, D., Ziese, U., Holz, I., Kristjansson, J. K., and Zillig, W. (1999). A novel virus family, the Rudiviridae: structure, virus-host interactions and genome variability of the sulfolobus viruses SIRV1 and SIRV2. Genetics 152, 1387–1396.Google Scholar
  159. Prangishvili, D., Vestergaard, G., Häring, M., Aramayo, R., Basta, T., Rachel, R., and Garrett, R.A. (2006a). Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J Mol Biol 359, 1203–1216.Google Scholar
  160. Prangishvili, D., Forterre, P., and Garrett, R.A. (2006b). Viruses of the Archaea: A unifying view. Nat Rev Microbiol 4, 837–848.Google Scholar
  161. Prangishvili, D., and Krupovic, M. (2012). A new proposed taxon for double-stranded DNA viruses, the order “Ligamenvirales”. Arch Virol 157, 791–795.Google Scholar
  162. Prangishvili, D. (2013). The wonderful world of archaeal viruses. Annu Rev Microbiol 67, 565–585.Google Scholar
  163. Proctor, L.M., and Fuhrman, J.A. (1990). Viral mortality of marine bacteria and cyanobacteria. Nature 343, 60–62.Google Scholar
  164. Rao, Y., and Su, J. (2015). Insights into the Antiviral Immunity against Grass Carp (Ctenopharyngodon idella) Reovirus (GCRV) in Grass Carp. J Immunol Res 2015, 1–18.Google Scholar
  165. Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., La Scola, B., Suzan, M., and Claverie, J.M. (2004). The 1.2-megabase genome sequence of mimivirus. Science 306, 1344–1350.Google Scholar
  166. Raoult, D., and Forterre, P. (2008). Redefining viruses: Lessons from mimivirus. Nat Rev Micro 6, 315–319.Google Scholar
  167. Rastrojo, A., and Alcamí, A. (2017). Aquatic viral metagenomics: lights and shadows. Virus Res 239, 87–96.Google Scholar
  168. Rensen, E.I., Mochizuki, T., Quemin, E., Schouten, S., Krupovic, M., and Prangishvili, D. (2016). A virus of hyperthermophilic archaea with a unique architecture among DNA viruses. Proc Natl Acad Sci USA 113, 2478–2483.Google Scholar
  169. Rice, G., Tang, L., Stedman, K., Roberto, F., Spuhler, J., Gillitzer, E., Johnson, J.E., Douglas, T., and Young, M. (2004). From The Cover: The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proc Natl Acad Sci USA 101, 7716–7720.Google Scholar
  170. Roberts, R.J. (2012). Fish Pathology. (Blackwell Publishing Ltd), pp186–291.Google Scholar
  171. Rohwer, F., and Edwards, R. (2002). The phage proteomic tree: a genomebased taxonomy for phage. J Bacteriology 184, 4529–4535.Google Scholar
  172. Rohwer, F., and Thurber, R.V. (2009). Viruses manipulate the marine environment. Nature 459, 207–212.Google Scholar
  173. Roossinck, M.J. (2011). The good viruses: viral mutualistic symbioses. Nat Rev Micro 9, 99–108.Google Scholar
  174. Roux, S., Brum, J.R., Dutilh, B.E., Sunagawa, S., Duhaime, M.B., Loy, A., Poulos, B.T., Solonenko, N., Lara, E., Poulain, J., et al. (2016). Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693.Google Scholar
  175. Safferman, R.S., Cannon, R.E., Desjardins, P.R., Gromov, B.V., Haselkorn, R., Sherman, L.A., and Shilo, M. (1983). Classification and nomenclature of viruses of cyanobacteria. Intervirology 19, 61–66.Google Scholar
  176. San Martín. C., Huiskonen, J.T., Bamford, J.K., Butcher, S.J., Fuller, S.D., Bamford, D.H., and Burnett, R.M. (2002). Minor proteins, mobile arms and membrane-capsid interactions in the bacteriophage PRD1 capsid. Nat Struct Biol 9, 756–763.Google Scholar
  177. Schleper, C., Kubo, K., and Zillig, W. (1992). The particle SSV1 from the extremely thermophilic archaeon Sulfolobus is a virus: demonstration of infectivity and of transfection with viral DNA. Proc Natl Acad Sci USA 89, 7645–7649.Google Scholar
  178. Schulz, F., Yutin, N., Ivanova, N.N., Ortega, D.R., Lee, T.K., Vierheilig, J., Daims, H., Horn, M., Wagner, M., Jensen, G.J., et al. (2017). Giant viruses with an expanded complement of translation system components. Science 356, 82–85.Google Scholar
  179. Shestakov, S.V., and Karbysheva, E.A. (2015). The role of viruses in the evolution of cyanobacteria. Biol Bull Rev 5, 527–537.Google Scholar
  180. Sheyn, U., Rosenwasser, S., Ben-Dor, S., Porat, Z., and Vardi, A. (2016). Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. ISME J 10, 1742–1754.Google Scholar
  181. Shi, M., Lin, X.D., Chen, X., Tian, J.H., Chen, L.J., Li, K., Wang, W., Eden, J.S., Shen, J.J., Liu, L., et al. (2018). The evolutionary history of vertebrate RNA viruses. Nature 556, 197–202.Google Scholar
  182. Short, S.M. (2012). The ecology of viruses that infect eukaryotic algae. Environ Microbiol 14, 2253–2271.Google Scholar
  183. Sibley, S.D., Finley, M.A., Baker, B.B., Puzach, C., Armién, A.G., Giehtbrock, D., and Goldberg, T.L. (2016). Novel reovirus associated with epidemic mortality in wild largemouth bass (Micropterus salmoides). J General Virology 8, 2482–2487.Google Scholar
  184. Steward, G.F., Culley, A.I., and Wood-Charlson, E.M. (2013). Marine viruses. In Encyclopedia of biodiversity, vol 5. Levin, S.A. ed, (Elsevier, London, UK), pp 127–144.Google Scholar
  185. Stevens, K., Weynberg, K., Bellas, C., Brown, S., Brownlee, C., Brown, M. T., and Schroeder, D.C. (2014). A novel evolutionary strategy revealed in the phaeoviruses. PLoS ONE 9, e86040.Google Scholar
  186. Sullivan, M.B., Coleman, M.L., Weigele, P., Rohwer, F., and Chisholm, S. W. (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3, e144.Google Scholar
  187. Sullivan, M.B., Huang, K.H., Ignacio-Espinoza, J.C., Berlin, A.M., Kelly, L., Weigele, P.R., DeFrancesco, A.S., Kern, S.E., Thompson, L.R., Young, S., et al. (2010). Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ MicroBiol 12, 3035–3056.Google Scholar
  188. Sullivan, M.B., Lindell, D., Lee, J.A., Thompson, L.R., Bielawski, J.P., and Chisholm, S.W. (2006). Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4, e234.Google Scholar
  189. Sullivan, M.B., Weitz, J.S., and Wilhelm, S. (2017). Viral ecology comes of age. Environ MicroBiol Rep 9, 33–35.Google Scholar
  190. Suttle, C.A. (2005). Viruses in the sea. Nature 437, 356–361.Google Scholar
  191. Suttle, C.A. (2007). Marine viruses — major players in the global ecosystem. Nat Rev Microbiol 5, 801–812.Google Scholar
  192. Syvanen, M. (2012). Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46, 341–358.Google Scholar
  193. Thingstad, T.F., Våge, S., Storesund, J.E., Sandaa, R.A., and Giske, J. (2014). A theoretical analysis of how strain-specific viruses can control microbial species diversity. Proc Natl Acad Sci USA 111, 7813–7818.Google Scholar
  194. Titilade, P.R., and Olalekan, E.I. (2015). The importance of marine genomics to life. J Ocean Res 3, 1–13.Google Scholar
  195. Tzipilevich, E., Habusha, M., and Ben-Yehuda, S. (2017). Acquisition of phage sensitivity by bacteria through exchange of phage receptors. Cell 168, 186–199.e12.Google Scholar
  196. Van Duin, J., and Tsareva, N. 2006. Single-stranded RNA phages. Chapter 15. In Calendar, R.L. The Bacteriophages (Oxford University Press), pp175–196.Google Scholar
  197. Van Etten, J.L. and Graves M.V. (2008). Phycodnaviruses. In Encyclopedia of Virology. Mahy, B.W.J. and Van Regenmortel, M.H.V. ed. (Academic Press), pp 116–125.Google Scholar
  198. Van Etten, J.L., and Dunigan, D.D. (2012). Chloroviruses: not your everyday plant virus. Trends Plant Sci 17, 1–8.Google Scholar
  199. 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, 861–865.Google Scholar
  200. Vaux, F., Trewick, S.A., and Morgan-Richards, M. (2017). Speciation through the looking-glass. Biol J Linn Soc 120, 480–488.Google Scholar
  201. Vestergaard, G., Aramayo, R., Basta, T., Häring, M., Peng, X., Brügger, K., Chen, L., Rachel, R., Boisset, N., Garrett, R.A., et al. (2008). Structure of the acidianus filamentous virus 3 and comparative genomics of related archaeal lipothrixviruses. J Virology 82, 371–381.Google Scholar
  202. Weinbauer, M.G. (2004). Ecology of prokaryotic viruses. FEMS Microbiol Rev 28, 127–181.Google Scholar
  203. Weitz, J.S., Stock, C.A., Wilhelm, S.W., Bourouiba, L., Coleman, M.L., Buchan, A., Follows, M.J., Fuhrman, J.A., Jover, L.F., Lennon, J.T., et al. (2015). A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J 9, 1352–1364.Google Scholar
  204. Weynberg, K.D., Allen, M.J., and Wilson, W.H. (2017). Marine prasinoviruses and their tiny plankton hosts: a review. Viruses 9, 43.Google Scholar
  205. Whitman, W.B., Coleman, D.C., and Wiebe, W.J. (1998). Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95, 6578–6583.Google Scholar
  206. Wigington, C.H., Sonderegger, D., Brussaard, C.P.D., Buchan, A., Finke, J. F., Fuhrman, J.A., Lennon, J.T., Middelboe, M., Suttle, C.A., Stock, C., et al. (2016). Re-examination of the relationship between marine virus and microbial cell abundances. Nat Microbiol 1, 15024.Google Scholar
  207. Wilhelm, S.W., and Suttle, C.A. (1999). Viruses and nutrient cycles in the sea. Bioscience 49, 781–788.Google Scholar
  208. Wilhelm, S.W., and Matteson, A.R. (2008). Freshwater and marine virioplankton: a brief overview of commonalities and differences. Freshwater Biol 53, 1076–1089.Google Scholar
  209. Wilhelm, S.W., Coy, S.R., Gann, E.R., Moniruzzaman, M., and Stough, J. M.A. (2016). Standing on the shoulders of giant viruses: five lessons learned about large viruses infecting small eukaryotes and the opportunities they create. PLoS Pathog 12, e1005752.Google Scholar
  210. Williams, T., Barbosa-Solomieu, V., and Chinchar, V.G. (2005). A decade of advances in iridovirus research. Adv Virus Res 65, 173–248.Google Scholar
  211. Wilson, W.H., Gilg, I.C., Moniruzzaman, M., Field, E.K., Koren, S., LeCleir, G.R., Martínez Martínez, J., Poulton, N.J., Swan, B.K., Stepanauskas, R., et al. (2017). Genomic exploration of individual giant ocean viruses. ISME J 11, 1736–1745.Google Scholar
  212. Wommack, K.E., and Colwell, R.R. (2000). Virioplankton: Viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64, 69–114.Google Scholar
  213. Woo, P.T.K., and Bruno, D.W. (2011). Fish Diseases and Disorders: Viral, Bacterial and Fungal Infections v.3. (CABI. UK), pp877.Google Scholar
  214. Yasuike, M., Nishiki, I., Iwasaki, Y., Nakamura, Y., Fujiwara, A., Sugaya, E., Kawato, Y., Nagai, S., Kobayashi, T., Ototake, M., et al. (2015). Full-genome sequence of a novel myovirus, GF-2, infecting Edwardsiellatarda: comparison with other Edwardsiella myoviral genomes. Arch Virol 160, 2129–2133.Google Scholar
  215. Yau, S., Lauro, F.M., DeMaere, M.Z., Brown, M.V., Thomas, T., Raftery, M.J., Andrews-Pfannkoch, C., Lewis, M., Hoffman, J.M., Gibson, J.A., et al. (2011). Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci USA 108, 6163–6168.Google Scholar
  216. Yolken, R.H., Jones-Brando, L., Dunigan, D.D., Kannan, G., Dickerson, F., Severance, E., Sabunciyan, S., Conover Talbot Jr., C., Prandovszky, E., Gurnon, J.R., et al. (2014). Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice. Proc Natl Acad Sci USA 111, 16106–16111.Google Scholar
  217. Zauberman, N., Mutsafi, Y., Halevy, D.B., Shimoni, E., Klein, E., Xiao, C., Sun, S., and Minsky, A. (2008). Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol 6, e114.Google Scholar
  218. Zhang, Q.Y. (2014). Advances in studies on biodiversity of cyanophages. Microbiol China, 41, 545–559.Google Scholar
  219. Zhang, Q.Y., and Gui, J.F. (2008). Aquatic Virology. (Higher Education Press, Beijing), pp1–414.Google Scholar
  220. Zhang, Q.Y., and Gui, J.F. (2009). One kind of strategic bio-resources that cannot be ignored—Freshwater and marine viruses and their roles in the global ecosystem. Bull Chinese Academy Sci 24, 520–526.Google Scholar
  221. Zhang, Q.Y., and Gui, J.F. (2012). Atlas of Aquatic Viruses and Viral Diseases. (Science Press, Beijing), pp1–479.Google Scholar
  222. Zhang, Q.Y., and Gui, J.F. (2015). Virus genomes and virus-host interactions in aquaculture animals. Sci China Life Sci 58, 156–169.Google Scholar
  223. Zhang, R., Wei, W., and Cai, L. (2014). The fate and biogeochemical cycling of viral elements. Nat Rev Micro 12, 850–851.Google Scholar
  224. Zhou, J., Sun, D., Childers, A., McDermott, T.R., Wang, Y., and Liles, M.R. (2015). Three novel virophage genomes discovered from yellowstone lake metagenomes. J Virol 89, 1278–1285.Google Scholar
  225. Zimmer, C., (2011). A Planet of Viruses. (The University of Chicago Press. Chicago), pp 128.Google Scholar
  226. Ziv, C., Malitsky, S., Othman, A., Ben-Dor, S., Wei, Y., Zheng, S., Aharoni, A., Hornemann, T., and Vardi, A. (2016). 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.Google Scholar

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© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, College of Modern Agriculture SciencesUniversity of Chinese Academy of Sciences, The Innovative Academy of Seed Design, Chinese Academy of SciencesWuhanChina
  2. 2.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiChina

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