Skip to main content
Log in

Diversity, evolutionary contribution and ecological roles of aquatic viruses

  • Review
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Avarre, J.C. (2017). Editorial: molecular tracing of aquatic viruses: where epidemiology needs to meet genomics. Front Microbiol 8, 1498.

    Article  PubMed  PubMed Central  Google Scholar 

  • Avrani, S., Schwartz, D.A., and Lindell, D. (2012). Virus-host swinging party in the oceans. Mobile Genet Elem 2, 88–95.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Beckett, S.J., and Williams, H.T.P. (2013). Coevolutionary diversification creates nested-modular structure in phage-bacteria interaction networks. Interface Focus 3, 20130033.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Beraldi-Campesi, H. (2013). Early life on land and the first terrestrial ecosystems. Ecol Process 2, 1.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Berliner, A.J., Mochizuki, T., and Stedman, K.M. (2018). Astrovirology: viruses at large in the universe. Astrobiology 18, 207–223.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Breitbart, M., and Rohwer, F. (2005). Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13, 278–284.

    Article  CAS  PubMed  Google Scholar 

  • Breitbart, M., Bonnain, C., Malki, K., and Sawaya, N.A. (2018). Phage puppet masters of the marine microbial realm. Nat Microbiol 3, 754–766.

    Article  CAS  PubMed  Google Scholar 

  • Breitbart, M., Thompson, L., Suttle, C., and Sullivan, M. (2007). Exploring the vast diversity of marine viruses. Oceanography 20, 135–139.

    Article  Google Scholar 

  • Breitbart, M. (2012). Marine viruses: Truth or dare. Annu Rev Mar Sci 4, 425–448.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Cavicchioli, R., and Erdmann, S. (2015). The discovery of Antarctic RNA viruses: a new game changer. Mol Ecol 24, 4809–4811.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claverie, J.M. (2006). Viruses take center stage in cellular evolution.. Genome Biol 7, 110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claverie, J.M., and Abergel, C. (2009). Mimivirus and its virophage. Annu Rev Genet 43, 49–66.

    Article  CAS  PubMed  Google Scholar 

  • Claverie, J.M., Abergel, C., and Ogata, H. (2009). Mimivirus. Curr Top Microbiol Immunol 328, 89–121.

    CAS  PubMed  Google Scholar 

  • Claverie, J.M., and Abergel, C. (2010). Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genets 26, 431–437.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Culley, A.I., Lang, A.S., and Suttle, C.A. (2006). Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–1798.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Edwards, R.A., and Rohwer, F. (2005). Viral metagenomics. Nat Rev Micro 3, 504–510.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Filée, J. (2015). Genomic comparison of closely related Giant Viruses supports an accordion-like model of evolution. Front Microbiol 6, 593.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Forterre, P., Krupovic, M., and Prangishvili, D. (2014). Cellular domains and viral lineages. Trends Micro Biol 22, 554–558.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Fuhrman, J.A. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez, P., and Buckling, A. (2011). Bacteria-phage antagonistic coevolution in soil. Science 332, 106–109.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffin, D.W. (2013). The quest for extraterrestrial life: what about the viruses? Astrobiology 13, 774–783.

    Article  PubMed  Google Scholar 

  • Gui, L., Chinchar, V.G., and Zhang, Q. (2018). Molecular basis of pathogenesis of emerging viruses infecting aquatic animals. Aquaculture Fisheries 3, 1–5.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Hugenholtz, P., and Tyson, G.W. (2008). Metagenomics. Nature 455, 481–483.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A.L., and Friedman, R. (2005). Poxvirus genome evolution by gene gain and loss. Mol PhyloGenets Evol 35, 186–195.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hurwitz, B.L., and U’Ren, J.M. (2016). Viral metabolic reprogramming in marine ecosystems. Curr Opin MicroBiol 31, 161–168.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Koonin, E.V. (2016). Viruses and mobile elements as drivers of evolutionary transitions. Phil Trans R Soc B 371, 20150442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Leslie, M. (2017). Cell-like giant viruses found. Science 356, 15–16.

    Article  CAS  PubMed  Google Scholar 

  • Li, S., Ou, T., and Zhang, Q. (2013). Two virus-like particles that cause lytic infections in freshwater cyanobacteria. Virol Sin 28, 303–305.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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).

    CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Mahy, B.W.J., and Van Regenmortel, M.H.V., (2008). Encyclopedia of Virology (2rd edit. Elsevier: Oxford, UK), pp159, 168–170.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. (2003). Bacterial photosynthesis genes in a virus. Nature 424, 741.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Middelboe, M., and Brussaard, C.P.D. (2017). Marine viruses: key players in marine ecosystems. Viruses 9, 302.

    Article  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  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 Res 19, 1441–1449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira, D., and Brochier-Armanet, C. (2008). Giant viruses, giant chimeras: the multiple evolutionary histories of mimivirus genes. BMC Evol Biol 8, 12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira, D., and López-García, P. (2009). Ten reasons to exclude viruses from the tree of life. Nat Rev Micro 7, 306–311.

    Article  CAS  Google Scholar 

  • 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 

  • Munn, C. (2011). Marine Microbiology: Ecology and Applications, 2nd ed. chapter 1 Microbes in the marine environment. (Garland Science, New York), pp1–23.

    Book  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Nagasaki, K. (2008). Dinoflagellates, diatoms, and their viruses. J Microbiol 46, 235–243.

    Article  PubMed  Google Scholar 

  • Ogata, H., and Claverie, J.M. (2007). Unique genes in giant viruses: regular substitution pattern and anomalously short size. Genome Res 17, 1353–1361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortmann, A.C., Wiedenheft, B., Douglas, T., and Young, M. (2006). Hot crenarchaeal viruses reveal deep evolutionary connections. Nat Rev Micro 4, 520–528.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Paerl, H.W., and Otten, T.G. (2013). Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65, 995–1010.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pearson, H. (2008). ‘Virophage’ suggests viruses are alive. Nature 454, 677.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Peduzzi, P. (2016). Virus ecology of fluvial systems: a blank spot on the map? Biol Rev 91, 937–949.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pennisi, E. (2013). Ever-bigger viruses shake tree of life. Science 341, 226–227.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plumb, J.A., and Hanson, L.A. ed. (2011). Health Maintenance and Principal Microbial Diseases of Cultured Fishes. (Wiley-Blackwell Oxford, UK), pp227–272.

    Book  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Prangishvili, D., Forterre, P., and Garrett, R.A. (2006b). Viruses of the Archaea: A unifying view. Nat Rev Microbiol 4, 837–848.

    Article  CAS  PubMed  Google Scholar 

  • Prangishvili, D., and Krupovic, M. (2012). A new proposed taxon for double-stranded DNA viruses, the order “Ligamenvirales”. Arch Virol 157, 791–795.

    Article  CAS  PubMed  Google Scholar 

  • Prangishvili, D. (2013). The wonderful world of archaeal viruses. Annu Rev Microbiol 67, 565–585.

    Article  CAS  PubMed  Google Scholar 

  • Proctor, L.M., and Fuhrman, J.A. (1990). Viral mortality of marine bacteria and cyanobacteria. Nature 343, 60–62.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Raoult, D., and Forterre, P. (2008). Redefining viruses: Lessons from mimivirus. Nat Rev Micro 6, 315–319.

    Article  CAS  Google Scholar 

  • Rastrojo, A., and Alcamí, A. (2017). Aquatic viral metagenomics: lights and shadows. Virus Res 239, 87–96.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts, R.J. (2012). Fish Pathology. (Blackwell Publishing Ltd), pp186–291.

    Book  Google Scholar 

  • Rohwer, F., and Edwards, R. (2002). The phage proteomic tree: a genomebased taxonomy for phage. J Bacteriology 184, 4529–4535.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Roossinck, M.J. (2011). The good viruses: viral mutualistic symbioses. Nat Rev Micro 9, 99–108.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Shestakov, S.V., and Karbysheva, E.A. (2015). The role of viruses in the evolution of cyanobacteria. Biol Bull Rev 5, 527–537.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Short, S.M. (2012). The ecology of viruses that infect eukaryotic algae. Environ Microbiol 14, 2253–2271.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan, M.B., Weitz, J.S., and Wilhelm, S. (2017). Viral ecology comes of age. Environ MicroBiol Rep 9, 33–35.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Suttle, C.A. (2007). Marine viruses — major players in the global ecosystem. Nat Rev Microbiol 5, 801–812.

    Article  CAS  PubMed  Google Scholar 

  • Syvanen, M. (2012). Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46, 341–358.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Titilade, P.R., and Olalekan, E.I. (2015). The importance of marine genomics to life. J Ocean Res 3, 1–13.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • Van Etten, J.L., and Dunigan, D.D. (2012). Chloroviruses: not your everyday plant virus. Trends Plant Sci 17, 1–8.

    Article  CAS  PubMed  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, 861–865.

    Article  CAS  PubMed  Google Scholar 

  • Vaux, F., Trewick, S.A., and Morgan-Richards, M. (2017). Speciation through the looking-glass. Biol J Linn Soc 120, 480–488.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Weinbauer, M.G. (2004). Ecology of prokaryotic viruses. FEMS Microbiol Rev 28, 127–181.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Weynberg, K.D., Allen, M.J., and Wilson, W.H. (2017). Marine prasinoviruses and their tiny plankton hosts: a review. Viruses 9, 43.

    Article  CAS  PubMed Central  Google Scholar 

  • Whitman, W.B., Coleman, D.C., and Wiebe, W.J. (1998). Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95, 6578–6583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm, S.W., and Suttle, C.A. (1999). Viruses and nutrient cycles in the sea. Bioscience 49, 781–788.

    Article  Google Scholar 

  • Wilhelm, S.W., and Matteson, A.R. (2008). Freshwater and marine virioplankton: a brief overview of commonalities and differences. Freshwater Biol 53, 1076–1089.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams, T., Barbosa-Solomieu, V., and Chinchar, V.G. (2005). A decade of advances in iridovirus research. Adv Virus Res 65, 173–248.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wommack, K.E., and Colwell, R.R. (2000). Virioplankton: Viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64, 69–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woo, P.T.K., and Bruno, D.W. (2011). Fish Diseases and Disorders: Viral, Bacterial and Fungal Infections v.3. (CABI. UK), pp877.

    Book  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Q.Y. (2014). Advances in studies on biodiversity of cyanophages. Microbiol China, 41, 545–559.

    CAS  Google Scholar 

  • Zhang, Q.Y., and Gui, J.F. (2008). Aquatic Virology. (Higher Education Press, Beijing), pp1–414.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Zhang, Q.Y., and Gui, J.F. (2012). Atlas of Aquatic Viruses and Viral Diseases. (Science Press, Beijing), pp1–479.

    Google Scholar 

  • Zhang, Q.Y., and Gui, J.F. (2015). Virus genomes and virus-host interactions in aquaculture animals. Sci China Life Sci 58, 156–169.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, R., Wei, W., and Cai, L. (2014). The fate and biogeochemical cycling of viral elements. Nat Rev Micro 12, 850–851.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Zimmer, C., (2011). A Planet of Viruses. (The University of Chicago Press. Chicago), pp 128.

    Book  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jian-Fang Gui.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, QY., Gui, JF. Diversity, evolutionary contribution and ecological roles of aquatic viruses. Sci. China Life Sci. 61, 1486–1502 (2018). https://doi.org/10.1007/s11427-018-9414-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-018-9414-7

Keywords

Navigation