Skip to main content
Log in

Dinoflagellates, diatoms, and their viruses

  • Review
  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

Since the first discovery of the very high virus abundance in marine environments, a number of researchers were fascinated with the world of “marine viruses”, which had previously been mostly overlooked in studies on marine ecosystems. In the present paper, the possible role of viruses infecting marine eukaryotic microalgae is enlightened, especially summarizing the most up-to-the-minute information of marine viruses infecting bloom-forming dinoflagellates and diatoms. To author’s knowledge, ∼40 viruses infecting marine eukaryotic algae have been isolated and characterized to different extents. Among them, a double-stranded DNA (dsDNA) virus “HcV” and a single-stranded RNA (ssRNA) virus “HcRNAV” are the only dinoflagellate-infecting (lytic) viruses that were made into culture; their hosts are a bivalve-killing dinoflagellate Heterocapsa circularisquama. In this article, ecological relationship between H. circularisquama and its viruses is focused. On the other hand, several diatom-infecting viruses were recently isolated and partially characterized; among them, one is infectious to a pen-shaped bloom-forming diatom species Rhizosolenia setigera; some viruses are infectious to genus Chaetoceros which is one of the most abundant and diverse diatom group. Although the ecological relationships between diatoms and their viruses have not been sufficiently elucidated, viral infection is considered to be one of the significant factors affecting dynamics of diatoms in nature. Besides, both the dinoflagellate-infecting viruses and diatom-infecting viruses are so unique from the viewpoint of virus taxonomy; they are remarkably different from any other viruses ever reported. Studies on these viruses lead to an idea that ocean may be a treasury of novel viruses equipped with fascinating functions and ecological roles.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Allen, M.J., D.C. Schroeder, M.T. Holden, and W.H. Wilson. 2006. Evolutionary history of the coccolithoviridae. Mol. Biol. Evol. 23, 86–92.

    Article  PubMed  CAS  Google Scholar 

  • Attoui, H., F.M. Jaafar, M. Belhouchet, P. Micco, X. Lamballerie, and C.P.D. Brussaard. 2006. Micromonas pusilla reovirus: a new member of the family Reoviridae assigned to a novel proposed genus (Mimoreovirus). J. Gen. Virol. 87, 1375–1383.

    Article  PubMed  CAS  Google Scholar 

  • Baudoux, A.C. and C.P. Brussaard. 2005. Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa. Virology 341, 80–90.

    Article  PubMed  CAS  Google Scholar 

  • Bergh, Ø., K.Y. Børsheim, G. Bratbak, and M. Heldal. 1989. High abundance of viruses found in aquatic environments. Nature 340, 467–468.

    Article  PubMed  CAS  Google Scholar 

  • Bettarel, Y., J. Kan, K. Wang, S. Cooney, K. Williamson, F. Chen, E. Wommack, and W. Coats. 2005. Isolation and characterisation of a small nuclear inclusion virus infecting the diatom Chaetoceros cf. gracilis. Aquat. Microb. Ecol. 40, 103–114.

    Article  Google Scholar 

  • Bratbak, G., J.K. Egge, and M. Heldal. 1993. Viral mortality of the marine alga Emiliania huxlevi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93, 39–48.

    Article  Google Scholar 

  • Bratbak, G., A. Jacobsen, M. Heldal, K. Nagasaki, and F. Thingstad. 1998. Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat. Microb. Ecol. 16, 1–9.

    Article  Google Scholar 

  • Brussaard, C.P. 2004. Viral control of phytoplankton populations — a review. J. Eukaryot. Microbiol. 51, 125–138.

    Article  PubMed  Google Scholar 

  • Brussaard, C.P.D., G. Bratbak, A.C. Baudoux, and P. Ruardij. 2007. Phaeocystis and its interaction with viruses. Biogeochemistry 83, 201–215.

    Article  Google Scholar 

  • Brussaard, C.P.D., A.A.M. Noordeloos, R.A. Sandaa, M. Heldal, and G. Bratbak. 2004a. Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 319, 280–291.

    Article  PubMed  CAS  Google Scholar 

  • Brussaard, C.P.D., S.M. Short, C.F. Frederickson, and C.A. Suttle. 2004b. Isolation and phylogenetic analysis of novel viruses infecting the phytoplankton Phaeocystis globosa (Prymnesiophyceae). Appl. Environ. Microbiol. 70, 3700–3705.

    Article  PubMed  CAS  Google Scholar 

  • Bubeck, J.A. and A.J.P. Pfitzner. 2005. Isolation and characterization of a new type of chlorovirus that infects an endosymbiotic Chlorella strain of the heliozoon Acanthocystis turfacea. J. Gen. Virol. 86, 2871–2877.

    Article  PubMed  CAS  Google Scholar 

  • Castberg, T., R. Thyrhaug, A. Larsen, R.A. Sandaa, M. Heldal, J.L. Van Etten, and G. Bratbak. 2002. Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyceae). J. Phycol. 38, 767–774.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cottrell, M.T. and C.A. Suttle. 1991. Wide-spread and clonal variation in viruses which cause lysis of a cosmopolitan, eukaryote marine phytoplankter, Micromonas pusilla. Mar. Ecol. Prog. Ser. 78, 1–9.

    Article  Google Scholar 

  • Cottrell, M.T. and C.A. Suttle. 1995. Genetic diversity of algal viruses which lyse the photosynthetic picoflagellate Micromonas pusilla (Prasinophyceae). Appl. Environ. Microbiol. 61, 3088–3091.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Davy, S.K., S.G. Burchett, A.L. Dale, P. Davies, J.E. Davy, C. Muncke, O. Hoegh-Guldberg, and W.H. Wilson. 2006. Viruses: agents of coral disease? Dis. Aquat. Org. 69, 101–110.

    Article  PubMed  CAS  Google Scholar 

  • Delaroque, N., D.G. Müller, G. Bothe, T. Pohl, R. Knippers, and W. Boland. 2001. The complete DNA sequence of the Ectocarpus siliculosus Virus EsV-1 genome. Virology 287, 112–132.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald, L.A., M.V. Graves, X. Li, T. Feldblyum, J. Hartigan, and J.L. Van Etten. 2007a. Sequence and annotation of the 314-kb MT325 and the 321-kb FR483 viruses that infect Chlorella Pbi. Virology 358, 459–471.

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald, L.A., M.V. Graves, X. Li, T. Feldblyum, W.C. Nierman, and J.L. Van Etten. 2007b. Sequence and annotation of the 369-kb NY-2A and the 345-kb AR158 viruses that infect Chlorella NC64A. Virology 358, 472–484.

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald, L.A., M.V. Graves, X. Li, J. Hartigan, A.J.P. Pfitzner, E. Hoffart, and J.L. Van Etten. 2007c. Sequence and annotation of the 288-kb ATCV-1 virus that infects an endosymbiotic chlorella strain of the heliozoon Acanthocytis turfacea. Virology 362, 350–361.

    Article  PubMed  CAS  Google Scholar 

  • Franca, S. 1976. On the presence of virus-like particles in the dinoflagellate Gyrodinium resplendens (Hulburt). Protistologica 12, 425–430.

    Google Scholar 

  • Friess-Klebl, A.K., R. Knippers, and D.G. Müller. 1994. Isolation and characterization of a DNA virus infecting Feldmannia simplex (Phaeophyceae). J. Phycol. 30, 653–658.

    Article  CAS  Google Scholar 

  • Garry, R.T., P. Hearing, and E.M. Cosper. 1998. Characterization of a lytic virus infectious to the bloom-forming microalga Aureococcus anophagefferens (Pelagophyceae). J. Phycol. 34, 616–621.

    Article  Google Scholar 

  • Gastrich, M.D., J.A. Leigh-Bell, C.J. Gobler, O.R. Anderson, S.W. Wilhelm, and M. Bryan. 2004. Viruses as potential regulators of regional brown tide blooms caused by the alga, Aureococcus anophagefferens. Estuaries 27, 112–119.

    Article  Google Scholar 

  • Henry, E.C. and R.H. Meints. 1992. A persistent virus infection in Feldmannia (Phaeophyceae). J. Phycol. 28, 517–526.

    Article  Google Scholar 

  • Jacobsen, A., G. Bratbak, and M. Heldal. 1996. Isolation and characterization of a virus infecting Phaeocystis pouchetii (Prymnesiophyceae). J. Phycol. 32, 923–927.

    Article  Google Scholar 

  • Kapp, M., R. Knippers, and D.G. Müller. 1997. New members to a group of DNA viruses infecting brown algae. Phycol. Res. 45, 85–90.

    Article  CAS  Google Scholar 

  • Kawakami, H. and N. Kawakami. 1978. Behavior of a virus in a symbiotic system, Paramecium bursaria-zoochlorella. J. Protozool. 25, 217–225.

    Google Scholar 

  • Lang, A.S., A.I. Culley, and C.A. Suttle. 2004. Genome sequence and characterization of a virus (HaRNAV) related to picornalike viruses that infects the marine toxic bloom-forming alga Heterosigma akashiwo. Virology 320, 206–217.

    Article  PubMed  CAS  Google Scholar 

  • Lanka, S.T., M. Klein, U. Ramsperger, D.G. Müller, and R. Knippers. 1993. Genome structure of a virus infecting the marine brown alga Ectocarpus siliculosus. Virology 193, 802–811.

    Article  PubMed  CAS  Google Scholar 

  • Lawrence, J.E., C.P.D. Brussaard, and C.A. Suttle. 2006. Virus-specific responses of Heterosigma akashiwo to infection. Appl. Environ. Microbiol. 72, 7829–7834.

    Article  PubMed  CAS  Google Scholar 

  • Lawrence, J.E., A.M. Chan, and C.A. Suttle. 2001. A novel virus (HaNIV) causes lysis of the toxic bloom-forming alga Heterosigma akashiwo (Raphidophyceae). J. Phycol. 37, 216–222.

    Article  Google Scholar 

  • Li, Y., Z. Lu, L. Sun, S. Ropp, G.F. Kutish, D.L. Rock, and J.L. Van Etten. 1997. Analysis of 74 kb of DNA located at the right end of the 330-kb chlorella virus PBCV-1 genome. Virology 237, 360–377.

    Article  PubMed  CAS  Google Scholar 

  • Lohr, J., C.B. Munn, and W.H. Wilson. 2007. Characterization of a latent virus-like infection of symbiotic zooxanthellae. Appl. Environ. Microbiol. 73, 2976–2981.

    Article  PubMed  CAS  Google Scholar 

  • Maier, I., S. Wolf, N. Delaroque, D.G. Müller, and H. Kawai. 1998. A DNA virus infecting the marine brown alga Pilayella littoralis (Ectocarpales, Phaeophysceae) in culture. Eur. J. Phycol. 33, 213–220.

    Article  Google Scholar 

  • Mattox, K.R. and K.D. Stewart. 1972. Probable virus infections in four genera of green algae. Can. J. Microbiol. 18, 1620–1621.

    Article  PubMed  CAS  Google Scholar 

  • Mayer, J.A. and F.J.R. Taylor. 1979. A virus which lyses the marine nanoflagellate Micromonas pusilla. Nature 281, 299–301.

    Article  Google Scholar 

  • Meints, R.H., R.G. Ivey, A.M. Lee, and T.J. Choi. 2008. Identification of two virus integration sites in the brown alga Feldmannia chromosome. J. Virol. 82, 1407–1413.

    Article  PubMed  CAS  Google Scholar 

  • Meints, R.H., J.L. Van Etten, D. Kuczmarski, K. Lee, and B. Ang. 1981. Viral infection of the symbiotic chlorella-like alga present in Hydra viridis. Virology 113, 698–703.

    Article  PubMed  CAS  Google Scholar 

  • Mizumoto, H., Y. Tomaru, Y. Takao, Y. Shirai, and K. Nagasaki. 2007. Intraspecies host specificity of a single-stranded RNA virus infecting a marine photosynthetic protist is determined at the early steps of infection. J. Virol. 81, 1372–1378.

    Article  PubMed  CAS  Google Scholar 

  • Müller, D.G. 1991. Mendelian segregation of a virus genome during host meiosis in the marine brown alga Ectocarpus siliculosus. J. Plant Physiol. 137, 739–743.

    Google Scholar 

  • Müller, D.G., M. Kapp, and R. Knippers. 1998. Viruses in marine brown algae. Adv. Virus Res. 50, 49–67.

    Article  PubMed  Google Scholar 

  • Müller, D.G., M. Sengco, S. Wolf, M. Brautigam, C.E. Schmid, M. Kapp, and R. Knippers. 1996. Comparison of two DNA viruses infecting the marine brown algae Ectocarpus siliculosus and E. fasciculatus. J. Gen. Virol. 77, 2329–2333.

    Article  PubMed  Google Scholar 

  • Nagasaki, K., Y. Shirai, Y. Takao, H. Mizumoto, K. Nishida, and Y. Tomaru. 2005a. Comparison of genome sequences of single-stranded RNA viruses infecting the bivalve-killing dinoflagellate Heterocapsa circularisquama. Appl. Environ. Microbiol. 71, 8888–8894.

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki, K., Y. Shirai, Y. Tomaru, K. Nishida, and S. Pietrokovski. 2005b. Algal viruses with distinct intraspecies host specificities include identical intein elements. Appl. Environ. Microbiol. 71, 3599–3607.

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki, K., K. Tarutani, and M. Yamaguchi. 1999. Growth characteristics of Heterosigma akashiwo virus and its possible use as a microbiological agent for red tide control. Appl. Environ. Microbiol. 65, 898–902.

    PubMed  CAS  Google Scholar 

  • Nagasaki, K., Y. Tomaru, N. Katanozaka, Y. Shirai, K. Nishida, S. Itakura, and M. Yamaguchi. 2004a. Isolation and characterization of a novel single-stranded RNA virus infecting the bloom-forming diatom Rhizosolenia setigera. Appl. Environ. Microbiol. 70, 704–711.

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki, K., Y. Tomaru, K. Nakanishi, N. Hata, N. Katanozaka, and M. Yamaguchi. 2004b. Dynamics of Heterocapsa circularisquama (Dinophyceae) and its viruses in Ago Bay, Japan. Aquat. Microb. Ecol. 34, 219–226.

    Article  Google Scholar 

  • Nagasaki, K., Y. Tomaru, Y. Shirai, Y. Takao, and H. Mizumoto. 2006. Dinoflagellate-infecting viruses. J. Mar. Biol. Ass. U.K. 86, 469–474.

    Article  CAS  Google Scholar 

  • Nagasaki, K., Y. Tomaru, Y. Takao, K. Nishida, Y. Shirai, H. Suzuki, and T. Nagumo. 2005c. Previously unknown virus infects marine diatom. Appl. Environ. Microbiol. 71, 3528–3535.

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki, K., Y. Tomaru, K. Tarutani, N. Katanozaka, S. Yamanaka, H. Tanabe, and M. Yamaguchi. 2003. Growth characteristics and intra-species host specificity of a large virus infecting the dinoflagellate Heterocapsa circularisquama. Appl. Environ. Microbiol. 69, 2580–2586.

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki, K. and M. Yamaguchi. 1997. Isolation of a virus infectious to the harmful bloom causing microalga Heterosigma akashiwo (Raphidophyceae). Aquat. Microb. Ecol. 13, 135–140.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Proctor, L.M. and J.A. Fuhrman. 1991. Roles of viral infection in organic particle flux. Mar. Ecol. Prog. Ser. 69, 133–142.

    Article  Google Scholar 

  • Reisser, W., T. Klein, and B. Becker. 1988a. Studies on phycoviruses. 1. On the ecology of viruses attacking Chlorellae exsymbiotic from an European strain of Paramecium bursaria. Arch. Hydrobiol. 111, 575–583.

    Google Scholar 

  • Reisser, W., D.E. Burbank, S.M. Meints, R.H. Meints, B. Becker, and J.L. Van Etten. 1988b. A comparison of viruses infecting two different chlorella-like green algae. Virology 167, 143–149.

    Article  PubMed  CAS  Google Scholar 

  • Rohozinski, J., L.E. Girton, and J.L. Van Etten. 1989. Chlorella viruses contain linear nonpermuted double strand DNA genomes with covalently closed hairpin ends. Virology 168, 363–369.

    Article  PubMed  CAS  Google Scholar 

  • Sandaa, R.A., M. Heldal, T. Castberg, R. Thyrhaug, and G. Bratbak. 2001. Isolation and characterization of two viruses with large genome size infecting Chrysochromulina ericina (Prymnesiophyceae) and Pyramimonas orientalis (Prasinophyceae). Virology 290, 272–280.

    Article  PubMed  CAS  Google Scholar 

  • Schroeder, D.C., J. Oke, M. Hall, G. Malin, and W.H. Wilson. 2003. Virus succession observed during an Emiliania huxleyi bloom. Appl. Environ. Microbiol. 69, 2484–2490.

    Article  PubMed  CAS  Google Scholar 

  • Shirai, Y., Y. Takao, H. Mizumoto, Y. Tomaru, D. Honda, and K. Nagasaki. 2006. Genomic and phylogenetic analysis of a single-stranded RNA virus infecting Rhizosolenia setigera (Stramenopiles: Bacillariophyceae). J. Mar. Biol. Ass. U.K. 86, 475–483.

    Article  CAS  Google Scholar 

  • Shirai, Y., Y. Tomaru, Y. Takao, H. Suzuki, T. Nagumo, and K. Nagasaki. 2008. Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetocerostenuissimus Meunier. Appl. Environ. Microbiol. Article in Press.

  • Sicko-Goad, L. and G. Walker. 1979. Viroplasm and large virus-like particles in the dinoflagellate Gymnodinium ubberrimum. Protoplasm 99, 203–210.

    Article  Google Scholar 

  • Soyer, M.O. 1978. Particules de type viral et filaments trichocystoides chez les dinoflagelles. Protistologica 14, 53–58.

    Google Scholar 

  • Suttle, C.A. 2000. The ecological, evolutionary and geochemical consequences of viral infection of cyanobacteria and eukaryotic algae, p. 248–286. In C.J. Hurst (ed.), Viral Ecology, Academic Press, London, UK.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Suttle, C.A. and A.M. Chan. 1995. Viruses infecting the marine Prymnesiophyte Chrysochromulina spp.: isolation, preliminary characterization and natural abundance. Mar. Ecol. Prog. Ser. 118, 275–282.

    Article  Google Scholar 

  • Tai, V., J.E. Lawrence, A.S. Lang, A.M. Chan, A.I. Culley, and C.A. Suttle. 2003. Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J. Phycol. 39, 343–352.

    CAS  Google Scholar 

  • Tarutani, K., K. Nagasaki, S. Itakura, and M. Yamaguchi. 2001. Isolation of a virus infecting the novel shellfish-killing dinoflagellate Heterocapsa circularisquama. Aquat. Microb. Ecol. 23, 103–111.

    Article  Google Scholar 

  • Tarutani, K., K. Nagasaki, and M. Yamaguchi. 2000. Viral impacts on total abundance and clonal composition of the harmful bloom-forming phytoplankton Heterosigma akashiwo. Appl. Environ. Microbiol. 66, 4916–4920.

    Article  PubMed  CAS  Google Scholar 

  • Thingstad, T.F., M. Heldal, G. Bratbak, and I. Dundas. 1993. Are viruses important partners in pelagic food webs? Trends Ecol. Evol. 8, 209–213.

    Article  Google Scholar 

  • Tomaru, Y., N. Hata, T. Masuda, M. Tsuji, K. Igata, Y. Masuda, T. Yamatogi, M. Sakaguchi, and K. Nagasaki. 2007. Ecological dynamics of the bivalve-killing dinoflagellate Heterocapsa circularisquama and its infectious viruses in different locations of western Japan. Environ. Microbiol. 9, 1376–1383.

    Article  PubMed  Google Scholar 

  • Tomaru, Y., N. Katanozaka, K. Nishida, Y. Shirai, K. Tarutani, M. Yamaguchi, and K. Nagasaki. 2004a. Isolation and characterization of two distinct types of HcRNAV, a single-stranded RNA virus infecting the bivalve-killing microalga Heterocapsa circularisquama. Aquat. Microb. Ecol. 34, 207–218.

    Article  Google Scholar 

  • Tomaru, Y. and K. Nagasaki. 2004. Widespread occurrence of viruses lytic to the bivalve-killing dinoflagellate Heterocapsa circularisquama in the western coast of Japan. Plankton Biol. Ecol. 51, 1–6.

    Google Scholar 

  • Tomaru, Y., Y. Shirai, H. Suzuki, T. Nagumo, and K. Nagasaki. 2008. Isolation and characterization of a novel single-stranded DNA virus infecting a cosmopolitan marine diatom Chaetoceros debilis. Aquat. Microb. Ecol. 50, 103–112.

    Article  Google Scholar 

  • Tomaru, Y., K. Tarutani, M. Yamaguchi, and K. Nagasaki. 2004b. Quantitative and qualitative impacts of viral infection on a Heterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan. Aquat. Microb. Ecol. 34, 227–238.

    Article  Google Scholar 

  • Van Etten, J.L. 1995. Phycodnaviridae, p. 100–103. In F.A. Murphy, C.M. Fauquet, D.H.L. Bishop, S.A. Ghabrial, A.W. Jarvis, G.P. Martelli, M.A. Mayo, and M.D. Summers (eds.) Virus Taxonomy, Sixth report of the International Committee On Taxonomy of Viruses virus taxonomy. Springer-Verlag, Vienna & New York.

    Google Scholar 

  • Van Etten, J.L. 2000. Family Phycodnaviridae, p. 183–193. In M.H.V. Van Regenmortel, C.M. Fauquet, D.H.L. Bishop, E.B. Carstens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle, and R.B. Wickner (eds.), Virus taxonomy, 7th Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, Calif, USA.

    Google Scholar 

  • Van Etten, J.L., M.V. Graves, D.G. Muller, W. Boland, and N. Delaroque. 2002. Phycodnaviridae — large DNA algal viruses. Arch. Virol. 147, 1479–1516.

    Article  PubMed  CAS  Google Scholar 

  • Van Etten, J.L., L.C. Lane, and R.H. Meints. 1991. Viruses and virus-like particles of eukaryotic algae. Microbiol. Rev. 55, 586–620.

    PubMed  Google Scholar 

  • Van Etten, J.L. and R.H. Meints. 1999. Giant viruses infecting algae. Ann. Rev. Microbiol. 53, 447–494.

    Article  Google Scholar 

  • Van Etten, J.L., R.H. Meints, D.E. Burbank, D. Kuczmarski, D.A. Cuppels, and L.C. Lane. 1981. Isolation and characterization of a virus from the intracellular green alga symbiotic with Hydra viridis. Virology 113, 704–711.

    Article  PubMed  Google Scholar 

  • Van Etten, J.L., R.H. Meints, D. Kuczmarski, D.E. Burbank, and K. Lee. 1982. Viruses of symbiotic chlorella-like algae isolated from Paramecium bursaria and Hydra viridis. Proc. Natl. Acad. Sci. USA 79, 3867–3871.

    Article  PubMed  Google Scholar 

  • Waters, R.E. and A.T. Chan. 1982. Micromonas pusilla virus: the virus growth cycle and associated physiological events within the host cells: host range mutation. J. Gen. Virol. 63, 199–206.

    Article  Google Scholar 

  • Wilson, W.H., I. Francis, K. Rian, and S.K. Davy. 2001. Temperature induction of viruses in symbiotic dinoflagellates. Aquat. Microb. Ecol. 25, 99–102.

    Article  Google Scholar 

  • Wilson, W.H., D.C. Schroeder, M.J. Allen, M.T.G. Holden, J. Parkhill, B.G. Barrell, C. Churcher, N. Hamlin, K. Mungall, H. Norbertczak, M.A. Quail, C. Price, E. Rabbinowitsch, D. Walker, M. Craigon, D. Roy, and P. Ghaza. 2005a. Complete genome sequence and lytic phase transcription profile of a coccolithovirus. Science 5737, 1090–1092.

    Article  CAS  Google Scholar 

  • Wilson, W.H., D.C. Schroeder, J. Ho, and M. Canty. 2006. Phylogenetic analysis of PgV-102P, a new virus from the English Channel that infects Phacocystis globosa. J. Mar. Biol. Assoc. U.K. 86, 485–490.

    Article  CAS  Google Scholar 

  • Wilson, W.H., G.A. Tarran, D. Schroeder, M. Cox, J. Oke, and G. Malin. 2002. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. U.K. 82, 369–377.

    Article  Google Scholar 

  • Wilson, W.H., J.L. Van Etten, D.C. Schroeder, K. Nagasaki, C. Brussaard, N. Delaroque, G. Bratbak, and C. Suttle. 2005b. Phycodnaviridae, p. 163–175. In C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, and L.A. Ball (eds.), Virus taxonomy, 8th Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, Calif, USA.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yamada, T., N. Chuchird, T. Kawasaki, K. Nishida, and S. Hiramatsu. 1999. Chlorella viruses as a source of novel enzymes. J. Biosci. Bioeng. 88, 353–361.

    Article  PubMed  CAS  Google Scholar 

  • Yamada, T., H. Onimatsu, and J.L. Van Etten. 2006. Chlorella viruses. Adv. Virus Res. 66, 293–336.

    Article  PubMed  CAS  Google Scholar 

  • Yan, X., P.R. Chipman, T. Castberg, G. Bratbak, and T.S. Baker. 2005. The marine algal virus PpV01 has an icosahedral capsid with T = 219 quasisymmetry. J. Virol. 79, 9236–9243.

    Article  PubMed  CAS  Google Scholar 

  • Zingone, A. 1995. The role of viruses in the dynamics of phytoplankton blooms. Giorn. Bot. It. 129, 415–423.

    Google Scholar 

  • Zingone, A., F. Natale, E. Biffali, M. Borra, G. Forlani, and D. Sarno. 2006. Diversity in morphology, infectivity, molecular characteristics and induced host resistance between two viruses infecting Micromonas pusilla. Aquat. Microb. Ecol. 45, 1–14.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keizo Nagasaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nagasaki, K. Dinoflagellates, diatoms, and their viruses. J Microbiol. 46, 235–243 (2008). https://doi.org/10.1007/s12275-008-0098-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-008-0098-y

Keywords

Navigation