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Virus assembly inHincksia hincksiae (Ectocarpales, Phaeophyceae) An electron and fluorescence microscopic study

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Summary

The filamentous brown algaHincksia hincksiae can be infected by a large icosahedral double-stranded DNA virus (HincV-1). The virus shows extended latency and is replicated only in cells homologous to sporangia. Virus formation was studied by transmission electron microscopy, DAPI staining, and β-tubulin immunofluorescence. Inhibition of cytokineses results in multinucleate cells, which are the first indication of virus replication in productive cells; the microtubular cytoskeleton does not seem to be affected by the virus. Replication of viral DNA begins in the nuclei, which increase in size and eventually disintegrate. Virus assembly takes place in a mixed nucleo-/cytoplasm. Capsids bud from cisternae, which are interpreted as modified endoplasmic reticulum aggregated to virus assembly centres. The internal membranous component of the virus is thus derived from the endoplasmic reticulum. The particles are empty (electron translucent) when assembled, and the nucleoprotein core seems to be packaged subsequently through an opening in the capsid. A number of fine structural features not previously reported from brown algae and related to virus formation are described. Our results on Hincksia hincksiae virus are compared with observations made on various other icosahedral DNA viruses infecting eukaryotic algae and animals.

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Abbreviations

ASFV:

African swine fever virus

BSA:

bovine serum albumin

DAPI:

4′,6-diamidino-phenylindole

dsDNA:

double-stranded DNA

EGTA:

ethyleneglycol-bis-(b-amino-ethyl ether)-N,N′-tetraacetic acid

ER:

endoplasmic reticulum

FV-3:

frog virus 3

HEPES:

N-2-hydroxyethylpiperazine-N′-2-ethane sulfonic acid

HincV-1:

Hincksia hincksiae virus type 1

PBCV-1:

Paramecium bursaria Chlorella virus 1

PBS:

phosphate-buffered saline

rER:

rough endoplasmic reticulum

TBS:

Tris-buffered saline Tris tris-(hydroxymethyl)-aminomethane

VAC:

virus assembly centre

VLP:

virus-like particle

VPC:

virus-producing cell

References

  • Ardré F (1969) Contribution à l'étude des algues marines du Portugal 1. La Flore. Port Acta Biol 10B: 137–555

    Google Scholar 

  • Arzuza O, Urzainqui A, Díaz-Ruiz JR, Tabarés E (1992) Morphogenesis of African swine fever virus in monkey kidney cells after reversible inhibition of replication by cycloheximide. Arch Virol 124: 343–354

    Google Scholar 

  • Brookes SM, Dixon LK, Parkhouse RME (1996) Assembly of African swine fever virus: quantitative ultrastructural analysis in vitro and in vivo. Virology 224: 84–92

    Google Scholar 

  • Cardinal A (1964) Étude sur les ectocarpacées de la Manche. Beih Nova Hedw 15: 1–86

    Google Scholar 

  • Chen F, Suttle CA (1996) Evolutionary relationships among large double-stranded DNA viruses that infect microalgae and other organisms as inferred from DNA polymerase genes. Virology 219: 170–178

    Google Scholar 

  • Clitheroe SB, Evans LV (1974) Viruslike particles in the brown algaEctocarpus. J Ultrastruct Res 49: 211–217

    Google Scholar 

  • Cobbold C, Whittle JT, Wileman T (1996) Involvement of the endoplasmic reticulum in the assembly and envelopment of African swine fever virus. J Virol 70: 8382–8390

    Google Scholar 

  • Devauchelle G, Stoltz DB, Darcy-Tripier F (1985) Comparative ultrastructure of Iridoviridae. Curr Top Microbiol Immunol 116: 1–21

    Google Scholar 

  • García-Beato R, Salas ML, Viñuela E, Salas J (1992) Role of the host cell nucleus in the replication of African swine fever virus DNA. Virology 188: 637–649

    Google Scholar 

  • Goorha R (1982) Frog virus 3 DNA replication occurs in two stages. J Virol 43: 519–528

    Google Scholar 

  • Henry EC, Meints RH (1992) A persistent virus infection inFeldmannia (Phaeophyceae). J Phycol 28: 517–526

    Google Scholar 

  • Hess RT, Poinar GO Jr (1985) Iridoviruses infecting terrestrial isopods and nematodes. Curr Top Microbiol Immunol 116: 49–76

    Google Scholar 

  • Hoffman LR (1978) Virus-like particles inHydrurus (Chrysophyceae). J Phycol 14: 110–114

    Google Scholar 

  • —, Stanker LH (1976) Virus-like particles in the green algaCylindrocapsa. Can J Bot 54: 2827–2841

    Google Scholar 

  • Kapp M, Knippers R, Müller DG (1997) New members of a group of DNA viruses infecting brown algae. Phycol Res 45: 85–90

    Google Scholar 

  • Kelly DC, Vance DF (1973) The lipid content of two iridescent viruses. J Gen Virol 21: 417–423

    Google Scholar 

  • Lee RE (1971) Systemic viral material in the cells of the freshwater red algaSirodotia tenuissima (Holden) Skuja. J Cell Sci 8: 623–631

    Google Scholar 

  • Maier I, Rometsch E, Wolf S, Kapp M, Müller DG, Kawai H (1997) Passage of a marine brown algal DNA virus fromEctocarpus fasciculatus (Ectocarpales, Phaeophyceae) toMyriotrichia clavaeformis (Dictyosiphonales, Phaeophyceae): infection symptoms and recovery. J Phycol 33: 838–844

    Google Scholar 

  • - Wolf S, Delaroque N, Müller DG (1998) A DNA virus infecting the marine brown algaPilayella littoralis (Ectocarpales, Phaeophyceae) in culture. Eur J Phycol 33 (in press)

  • Markey DR (1974) A possible virus infection in the brown algaPylaiella littoralis. Protoplasma 80: 223–232

    Google Scholar 

  • Meints RH, Lee K, Van Etten JL (1986) Assembly site of the virus PBCV-1 in a Chlorella-like green alga: ultrastructural studies. Virology 154: 240–245

    Google Scholar 

  • Melkonian M (1982) Virus-like particles in the scaly green flagellateMesostigma viride. Br Phycol J 17: 63–68

    Google Scholar 

  • Müller DG, Kawai H, Stache B, Lanka S (1990) A viras infection in the marine brown algaEctocarpus siliculosus (Phaeophyceae). Bot Acta 103: 72–82

    Google Scholar 

  • —, Kapp M, Knippers R (1998) Viruses in marine brown algae. Adv Virus Res 50: 49–67

    Google Scholar 

  • Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) (1995) Virus taxonomy. Springer, Wien New York

    Google Scholar 

  • Nagasaki K, Ando M, Imai I, Itakura S, Ishida Y (1994) Virus-like particles inHeterosigma akashiwo (Raphidophyceae): a possible red tide disintegration mechanism. Mar Biol 119: 307–312

    Google Scholar 

  • Oliveira L, Bisalputra T (1978) A virus infection in the brown algaSorocarpus uvaeformis (Lyngbye) Pringsheim (Phaeophyta, Ectocarpales). Ann Bot 42: 439–445

    Google Scholar 

  • Parodi ER, Müller DG (1994) Field and culture studies on virus infections inHincksia hincksiae andEctocarpus fasciculatus (Ectocarpales, Phaeophyceae). Eur J Phycol 29: 113–117

    Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae: Proceedings of the U.S.-Japan Conference 1966, Hakone. Japanese Society for Plant Physiology, pp 63–75

  • Reisser W (1993) Viruses and virus-like particles of freshwater and marine eukaryotic algae: a review. Arch Protistenk 143: 257–265

    Google Scholar 

  • —, (1995) Phycovirology: aspects and prospect of a new phycological discipline. In: Wiessner W, Schnepf E, Starr RC (eds) Algae, environment and human affairs. Biopress, Bristol, pp 143–158

    Google Scholar 

  • Sicko-Goad L, Walker G (1979) Viroplasm and large virus-like particles in the dinoflagellateGymnodinium uberrimum. Protoplasma 99: 203–210

    Google Scholar 

  • Van Etten JL (1995) Giant Chlorella viruses. Mol Cells 5: 99–106

    Google Scholar 

  • —, Lane LC, Meints RH (1991) Viruses and viruslike particles of eukaryotic algae. Microbiol Rev 55: 586–620

    Google Scholar 

  • Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25: 407–408

    Google Scholar 

  • Viñuela E (1985) African swine fever virus. Curr Top Microbiol Immunol 116: 151–170

    Google Scholar 

  • Williams MA (1977) Quantitative methods in biology. In: Glauert AM (ed) Practical methods in electron microscopy, vol 6. North-Holland Biomedical Press, Amsterdam, p. 63

    Google Scholar 

  • Williams T (1996) The Iridoviruses. Adv Virus Res 46: 345–412

    Google Scholar 

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Authors and Affiliations

  1. Fakultät für Biologie, Universität Konstanz, D-78457, Konstanz, Federal Republic of Germany

    Susanne Wolf, I. Maier & D. G. Müller

  2. Institute of General Botany, University of Athens, Athens

    C. Katsaros

Authors
  1. Susanne Wolf
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  2. I. Maier
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  3. C. Katsaros
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  4. D. G. Müller
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Correspondence to Susanne Wolf.

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Wolf, S., Maier, I., Katsaros, C. et al. Virus assembly inHincksia hincksiae (Ectocarpales, Phaeophyceae) An electron and fluorescence microscopic study. Protoplasma 203, 153–167 (1998). https://doi.org/10.1007/BF01279472

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  • DOI: https://doi.org/10.1007/BF01279472

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