Coral Reefs

, Volume 27, Issue 3, pp 569–580 | Cite as

Prevalence of virus-like particles within a staghorn scleractinian coral (Acropora muricata) from the Great Barrier Reef

Report

Abstract

Transmission electron microscopy (TEM) was used to determine whether Acropora muricata coral colonies from the Great Barrier Reef (GBR), Australia, harboured virus-like particles (VLPs). VLPs were present in all coral colonies sampled at Heron Island (southern GBR) and in tagged coral colonies sampled in at least two of the three sampling periods at Lizard Island (northern GBR). VLPs were observed within gastrodermal and epidermal tissues, and on rarer occasions, within the mesoglea. These VLPs had similar morphologies to known prokaryotic and eukaryotic viruses in other systems. Icosahedral VLPs were observed most frequently, however, filamentous VLPs (FVLPs) and phage were also noted. There were no clear differences in VLP size, morphology or location within the tissues with respect to sample date, coral health status or site. The most common VLP morphotype exhibited icosahedral symmetry, 120–150 nm in diameter, with an electron-dense core and an electronlucent membrane. Larger VLPs of similar morphology were also common. VLPs occurred as single entities, in groups, or in dense clusters, either as free particles within coral tissues, or within membrane-bound vacuoles. VLPs were commonly observed within the perinuclear region, with mitochondria, golgi apparatus and crescent-shaped particles frequently observed within close proximity. The host(s) of these observed VLPs was not clear; however, the different sizes and morphologies of VLPs observed within A. muricata tissues suggest that viruses are infecting either the coral animal, zooxanthellae, intracellular bacteria and/or other coral-associated microbiota, or that the one host is susceptible to infection from more than one type of virus. These results add to the limited but emerging body of evidence that viruses represent another potentially important component of the coral holobiont.

Keywords

Coral reef Virus Microbial Electron microscopy VLP 

References

  1. Ackermann HA (2001) Frequency of morphological phage descriptions in the year 2000. Arch Virol 146:843–857PubMedCrossRefGoogle Scholar
  2. Ainsworth TD, Fine M, Blackall LL, Hoegh-Guldberg O (2006) Fluorescence in situ hybridisation and spectral imaging of coral-associated bacterial communities. Appl Environ Microbiol 72:3016–3020PubMedCrossRefGoogle Scholar
  3. Anders K, Yoshimizu M (1994) Role of viruses in the induction of skin tumours and tumour-like proliferations of fish. Dis Aquat Org 19:215–232CrossRefGoogle Scholar
  4. Anderson IG, Shariff M, Nash G, Nash M (1987) Mortalities of juvenile shrimp, Penaeus monodon, associated with Penaeus monodon baculovirus, cytoplasmic reo-like virus, rickettsia and bacterial infections, from Malaysian brackish water ponds. Asian Fish Sci 1:47–64Google Scholar
  5. Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55CrossRefGoogle Scholar
  6. Borsheim KY, Bratback G, Heldal M (1990) Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy. Appl Environ Microbiol 56:352–356PubMedGoogle Scholar
  7. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99:14250–14255PubMedCrossRefGoogle Scholar
  8. Brussaard CPD, Kempers RS, Kop AJ, Riegman R, Heldal M (1996) Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat Microb Ecol 10:105–113CrossRefGoogle Scholar
  9. Brussaard CPD, Noordeloos AAM, Sandaa RA, Heldal M, Bratbak G (2004) Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 319:280–291PubMedCrossRefGoogle Scholar
  10. Cervino JM, Hayes R, Goreau TJ, Smith GS (2004) Zooxanthellae regulation in yellow blotch/band and other coral diseases contrasted with temperature related bleaching: in situ destruction vs expulsion. Symbiosis 37:63–85Google Scholar
  11. Chen F, Suttle CA (1995) Amplification of DNA polymerase gene fragments from viruses infecting microalgae. Appl Environ Microbiol 61:1274–1278PubMedGoogle Scholar
  12. Culley AI, Lang AS, Suttle CA (2003) High diversity of unknown picorna-like viruses in the sea. Nature 424:1054–1057PubMedCrossRefGoogle Scholar
  13. Cusack RB, Groman DB, MacKinnon A-M, Kibenge FSB, Wadowska D, Brown N (2001) Pathology associated with an aquareovirus in captive juvenile Atlantic halibut Hippoglossus hippoglossus and an experimental treatment strategy for a concurrent bacterial infection. Dis Aquat Org 44:7–16PubMedCrossRefGoogle Scholar
  14. Davy JE, Patten NL (2007) Morphological diversity of virus-like particles within the surface microlayer of scleractinian corals. Aquat Microb Ecol 47:37–44CrossRefGoogle Scholar
  15. Davy SK, Burchett SG, Dale AL, Davies P, Davy JE, Muncke C, Hoegh-Guldberg O, Wilson WH (2006) Viruses: agents of coral disease? Dis Aquat Org 69:101–110PubMedCrossRefGoogle Scholar
  16. Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725CrossRefGoogle Scholar
  17. Elston R (1997) Special topic review: bivalve mollusc viruses. World J Microbiol Biotechnol 13:393–403CrossRefGoogle Scholar
  18. Essbauer S, Ahne W (2001) Viruses of lower invertebrates. J Vet Med Sci 48:403–475CrossRefGoogle Scholar
  19. Fuhrman JA (1999) Marine viruses and their biogeochemical effects. Nature 399:541–548PubMedCrossRefGoogle Scholar
  20. Guixa-Boixereu N, Lysnes K, Pedros-Alio C (1999) Viral lysis and bacterivory during a phytoplankton bloom in a coastal water microcosm. Appl Environ Microbiol 65:1949–1958PubMedGoogle Scholar
  21. Haebler R, Moeller RB Jr (1993) Pathobiology of selected marine mammal diseases. In: Couch JA, Fournie JW (eds) Pathobiology of marine and estuarine organisms. CRC Press, Boca Raton, pp 217–244Google Scholar
  22. Harrison PL (1990) Sperm morphology and fertilisation strategies in scleractinian corals, vol 5. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction, Elsevier Science Publishers, Amsterdam, pp 299–304Google Scholar
  23. ICTV (2005) 8th Report of the international committee on taxonomy of viruses. Online access: http://www.ncbi.nlm.nih.gov/ICTVdb/index.htm
  24. Jiang SC, Paul JH (1996) Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar Ecol Prog Ser 142:27–38CrossRefGoogle Scholar
  25. Kaczmarsky LT (2006) Coral disease dynamics in the central Philippines. Dis Aquat Org 69:9–21PubMedCrossRefGoogle Scholar
  26. Kaczmarsky LT, Richardson LL (2007) Transmission of growth anomalies between Indo-Pacific Porites corals. Dis Aquat Org 94:218–221Google Scholar
  27. Kazama FY, Schornstein KL (1972) Herpes-type virus particles associated with a fungus. Science 177:696–697PubMedCrossRefGoogle Scholar
  28. Kellogg CA (2004) Tropical archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88CrossRefGoogle Scholar
  29. Kramarsky-Winter E, Harel M, Siboni N, Dov BE, Brickner I, Loya Y, Kushmaro A (2006) Identification of a protist-coral association and its possible ecological role. Mar Ecol Prog Ser 317:67–73CrossRefGoogle Scholar
  30. Lemke A, Nash CA (1974) Fungal viruses. Bacteriol Rev 38:29–56PubMedGoogle Scholar
  31. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000PubMedCrossRefGoogle Scholar
  32. Lightner DV, Redman RM (1998) Shrimp diseases and current diagnostic methods. Aquaculture 164:201–220CrossRefGoogle Scholar
  33. Lohr J, Munn C, Wilson WH (2007) Characterisation of a latent virus-like infection of symbiotic zooxanthellae. Appl Environ Microbiol 73:2976–2981PubMedCrossRefGoogle Scholar
  34. Loya Y, Bull G, Pichon M (1984) Tumour formations in scleractinian corals. Helgol Wiss Meeresunters 37:99–112CrossRefGoogle Scholar
  35. Moestrup O, Thomsen HA (1974) An ultrastructural study of the flagellate Pyramimonas orientalis with particular emphasis on golgi apparatus activity and the flagellar apparatus. Protoplasma 81:247–269CrossRefGoogle Scholar
  36. Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H (2005) The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 102:16919–16926PubMedCrossRefGoogle Scholar
  37. Nagasaki K, Tomaru Y, Shirai Y, Takao Y, Mizumoto H (2006) Dinoflagellate-infecting viruses. J Mar Biol Assoc UK 86:469–474CrossRefGoogle Scholar
  38. Nagasaki K, Tomaru Y, Nakanishi K, Hata N, Katanozaka N, Yamaguchi M (2004) Dynamics of Heterocapsa circularisquama (Dinophyceae) and its viruses in Ago Bay, Japan. Aquat Microb Ecol 34:219–226CrossRefGoogle Scholar
  39. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C (2005) Viral factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97:147–172PubMedCrossRefGoogle Scholar
  40. Panek FM (2005) Epizootics and disease of coral reef fish in the tropical Western Atlantic and Gulf of Mexico. Rev Fish Sci 13:1–21CrossRefGoogle Scholar
  41. Paul JH, DeFlaun MF, Jeffrey WH (1986) Elevated levels of microbial activity in the coral surface microlayer. Mar Ecol Prog Ser 33:29–40CrossRefGoogle Scholar
  42. Pienaar RN (1976) Virus-like particles in three species of phytoplankton from San Juan Island, Washington. Phycologia 15:185–190Google Scholar
  43. Preisig HR, Hibberd DJ (1984) Virus-like particles and endophytic bacteria in Paraphysomonas and Chromophysomonas (Chrysophyceae). Nord J Bot 4:279–285CrossRefGoogle Scholar
  44. Proctor LM (1997) Advances in the study of marine viruses. Microsc Res Techniq 37:136–161CrossRefGoogle Scholar
  45. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  46. Rohwer F, Edwards R (2002) The phage proteomic tree; a genome based taxonomy for phages. J Bacteriol 184:4529–4535PubMedCrossRefGoogle Scholar
  47. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91CrossRefGoogle Scholar
  48. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  49. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbioses. Proc Natl Acad Sci USA 92:2850–2853PubMedCrossRefGoogle Scholar
  50. Rungger D, Rastelli M, Braendle E, Malsberger RG (1971) A viruslike particle associated with lesions in the muscles of Octopus vulgaris. J Invertebr Pathol 17:72–80CrossRefGoogle Scholar
  51. Sano E, Carlson S, Wegley L, Rohwer F (2004) Movement of viruses between biomes. Appl Environ Microbiol 70:5842–5846PubMedCrossRefGoogle Scholar
  52. Schroeder DC, Oke J, Malin G, Wilson WH (2002) Coccolithovirus (Phycodnaviridae): characterisation of a new large dsDNA algal virus that infects Emiliania huxleyi. Arch Virol 2002:1685–1698CrossRefGoogle Scholar
  53. Sicko-Goad L, Walker G (1979) Viroplasm and large virus-like particles in the dinoflagellate Gymnodinium uberrimum. Protoplasma 99:203–210CrossRefGoogle Scholar
  54. Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellae corals. Mar Ecol Prog Ser 266:273–302CrossRefGoogle Scholar
  55. Suttle CA (1994) The significance of viruses to mortality in aquatic microbial communities. Microb Ecol 28:237–243CrossRefGoogle Scholar
  56. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27CrossRefGoogle Scholar
  57. Van Etten JL, Cane LC, Meints RH (1991) Viruses and viruslike particles of eukaryotic algae. Microbiol Rev 55:586–620PubMedGoogle Scholar
  58. Wegley L, Edwards R, Rodriguez-Brito B, Lui H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719PubMedCrossRefGoogle Scholar
  59. Wegley L, Yu YN, Breitbart M, Casas V, Kline DI, Rohwer F (2004) Coral-associated archaea. Mar Ecol Prog Ser 273:89–96CrossRefGoogle Scholar
  60. Weil E, Smith G, Gil-Agudelo DL (2006) Status and progress in coral reef disease research. Dis Aquat Org 69:1–7PubMedCrossRefGoogle Scholar
  61. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181PubMedCrossRefGoogle Scholar
  62. Weinbauer MG, Peduzzi P (1994) Frequency, size and distribution of bacteriophages in different marine bacterial morphotypes. Mar Ecol Prog Ser 108:11–20CrossRefGoogle Scholar
  63. Willis BL, Page CA, Dinsdale EA (2004) Coral diseases on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, pp 69–104Google Scholar
  64. Wilson WH, Chapman DM (2001) Observation of virus-like particles in thin sections of the plumose anemone, Metridium senile. J Mar Biol Assoc UK 81:879–880CrossRefGoogle Scholar
  65. Wilson WH, Dale AL, Davy JE, Davy SK (2005) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148CrossRefGoogle Scholar
  66. Wilson WH, Francis I, Ryan K, Davy SK (2001) Temperature induction of viruses in symbiotic dinoflagellates. Aquat Microb Ecol 25:99–102CrossRefGoogle Scholar
  67. Yamashiro H, Yamamoto M, Van Woesik R (2000) Tumour formation on the coral Montipora informis. Dis Aquat Org 14:211–217CrossRefGoogle Scholar
  68. Yarden O, Ainsworth TD, Roff G, Leggat W, Fine M, Hoegh-Guldberg O (2007) Increased prevalence of ubiquitous ascomycetes in an acroporid coral (Acropora formosa) exhibiting symptoms of brown band syndrome and skeletal eroding band disease. Appl Eviron Microbiol 73:2755–2757CrossRefGoogle Scholar
  69. Zhong Y, Chen F, Wilhelm SW, Poorvin L, Hodson RE (2002) Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20. Appl Environ Microbiol 68:1576–1584PubMedCrossRefGoogle Scholar
  70. Zillig W, Prangishvilli D, Schleper C, Elferink M, Holz I, Albers S, Janekovic D, Götz D (1996) Viruses, plasmids and other genetic elements of thermophillic and hyperthermophilic Archaea. FEMS Microbiol Rev 18:225–236PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • N. L. Patten
    • 1
    • 2
  • P. L. Harrison
    • 1
  • J. G. Mitchell
    • 2
  1. 1.Coral Reef Research Centre, School of Environmental Science and ManagementSouthern Cross UniversityLismoreAustralia
  2. 2.School of Biological SciencesFlinders UniversityAdelaideAustralia

Personalised recommendations