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Prevalent and persistent viral infection in cultures of the coral algal endosymbiont Symbiodinium

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Abstract

Reef corals are under threat from bleaching and disease outbreaks that target both the host animal and the algal symbionts within the coral holobiont. A viral origin for coral bleaching has been hypothesized, but direct evidence has remained elusive. Using a multifaceted approach incorporating flow cytometry, transmission electron microscopy, DNA and RNA virome sequencing, we show that type C1 Symbiodinium cultures host a nucleocytoplasmic large double-stranded DNA virus (NCLDV) related to Phycodnaviridae and Mimiviridae, a novel filamentous virus of unknown phylogenetic affiliation, and a single-stranded RNA virus related to retroviruses. We discuss implications of these findings for laboratory-based experiments using Symbiodinium cultures.

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References

  • Angly FE, Willner D, Prieto-Davo A, Edwards RA, Schmieder R, Vega Thurber R, Antonopoulos DA, Barott K, Cottrell MT, Desnues C, Dinsdale EA, Furlan M, Haynes M, Henn MR, Hu YF, Kirchman DL, McDole T, McPherson JD, Meyer F, Miller RM, Mundt E, Naviaux RK, Rodriguez-Mueller B, Stevens R, Wegley L, Zhang LX, Zhu BL, Rohwer F (2009) The GAAS metagenomic tool and its estimations of viral and microbial average genome size in four major biomes. Plos Comp Biol 5:e1000593

    Article  Google Scholar 

  • Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20

    Article  PubMed  Google Scholar 

  • Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471

    Article  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesi VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bidle KD, Vardi A (2011) A chemical arms race at sea mediates algal host–virus interactions. Curr Opin Microbiol 14:449–457

    Article  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • Brussaard CPD (2004) Optimization of procedures for counting viruses by flow cytometry. Appl Environ Microbiol 70:1506–1513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa AMS, Welsh RM, Vega Thurber RL (2012) Unique nucleocytoplasmic dsDNA and +ssRNA viruses are associated with the dinoflagellate endosymbionts of corals. ISME J 7:13–27

    Article  PubMed  PubMed Central  Google Scholar 

  • Correa AMS, Ainsworth TD, Rosales SM, Thurber AR, Butler CR, Vega Thurber RL (2016) Viral outbreak in corals associated with an in situ bleaching event: atypical herpes-like viruses and a new megavirus infecting Symbiodinium. Front Microbiol 7:127

    Article  PubMed  PubMed Central  Google Scholar 

  • Culley AI, Suttle CA, Steward GF (2010) Characterization of the diversity of marine RNA viruses. In: Wilhelm SW, Weinbauer MG, Suttle CA (eds) Manual of aquatic viral ecology. American Society of Limnology and Oceanography Waco, TX

    Google Scholar 

  • Culley AI, Mueller JA, Belcaid M, Wood-Charlson EM, Poisson G, Steward GF (2014) The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. mBio 5:e01210-14

  • Davy JE, Patten NL (2007) Morphological diversity of virus-like particles within the surface microlayer of scleractinian corals. Aquat Microb Ecol 47:37–44

    Article  Google Scholar 

  • 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 Organ 69:101–110

    Article  CAS  PubMed  Google Scholar 

  • Downs CA, McDougall KE, Woodley CM, Fauth JE, Richmond RH, Kushmaro A, Gibb SW, Loya Y, Ostrander K, Kramarsky-Winter E (2013) Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching. PLoS One 8:e77173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunlap WC, Starcevic A, Baranasic D, Diminic J, Zucko J, Gacesa R, van Oppen MJH, Hranueli D, Cullum J, Long PF (2013) KEGG orthology-based annotation of the predicted proteome of Acropora digitifera: ZoophyteBase — an open access and searchable database of a coral genome. BMC Genomics 14:509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eakin CM, Lough JM, Heron SF (2009) Climate variability and change: monitoring data and evidence for increased coral bleaching stress. In: van Oppen MH, Lough JM (eds) coral bleaching. Springer, Berlin, Heidelberg

    Google Scholar 

  • Evans C, Malin G, Mills GP, Wilson WH (2006) Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J Phycol 42:1040–1047

    Article  CAS  Google Scholar 

  • Ferrier-Pagès C, Richard C, Forcioli D, Allemand D, Pichon M, Shick JM (2007) Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species. Biol Bull 213:76–87

    Article  PubMed  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120

    Article  Google Scholar 

  • Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Iyer LM, Aravind L, Koonin EV (2001) Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 75:11720–11734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iyer LM, Balaji S, Koonin EV, Aravind L (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117:156–184

    Article  CAS  PubMed  Google Scholar 

  • Kim FJ, Battini J-L, Manel N, Sitbon M (2004) Emergence of vertebrate retroviruses and envelope capture. Virology 318:183–191

    Article  CAS  PubMed  Google Scholar 

  • King A, Adams M, Carstens E, Lefkowitz E (2011) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego

    Google Scholar 

  • Laffy PW, Wood-Charlson EM, Turaev D, Weynberg KD, Botté ES, van Oppen MJH, Webster NS, Rattei T (2016) HoloVir: a workflow for investigating the diversity and function of viruses in invertebrate holobionts. Front Microbiol 7:822

    Article  PubMed  PubMed Central  Google Scholar 

  • Lang AS, Rise ML, Culley AI, Steward GF (2009) RNA viruses in the sea. FEMS Microbiol Rev 33:295–323

    Article  CAS  PubMed  Google Scholar 

  • Lawrence SA, Wilson WH, Davy JE, Davy SK (2014) Latent virus-like infections are present in a diverse range of Symbiodinium spp. (Dinophyta). J Phycol 50:977–997

    Article  Google Scholar 

  • Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377

    Article  Google Scholar 

  • Levin RA, Voolstra CR, Weynberg KD, van Oppen MJH (2016) Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J 11:808–812

    Article  PubMed  Google Scholar 

  • Lohr J, Munn CB, Wilson WH (2007) Characterization of a latent virus-like infection of symbiotic zooxanthellae. Appl Environ Microbiol 73:2976–2981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mokili JL, Rohwer F, Dutilh BE (2012) Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2:63–77

    Article  CAS  PubMed  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454–460

    Article  Google Scholar 

  • Onji M, Nakano S-I, Suzuki S (2003) Virus-like particles suppress growth of the red-tide-forming marine dinoflagellate Gymnodinium mikimotoi. Mar Biotech 5:435–442

    Article  CAS  Google Scholar 

  • Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral- associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  • Rosenberg E, Kushmaro A (2011) Microbial diseases of corals: pathology and ecology. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht

    Google Scholar 

  • Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin E, Yossi L (2009) The role of microorganisms in coral bleaching. ISME J 3:139–146

    Article  CAS  PubMed  Google Scholar 

  • Roux S, Tournayre J, Mahul A, Debroas D, Enault F (2014) Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinformatics 15:76

    Article  PubMed  PubMed Central  Google Scholar 

  • Sawyer SJ, Muscatine L (2001) Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 204:3443–3456

    CAS  PubMed  Google Scholar 

  • Steward GF, Culley AI, Mueller JA, Wood-Charlson EM, Belcaid M, Poisson G (2013) Are we missing half of the viruses in the ocean? ISME J 7:672–679

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Thomas V, Bertelli C, Collyn F, Casson N, Telenti A, Goesmann A, Croxatto A, Greub G (2011) Lausannevirus, a giant amoebal virus encoding histone doublets. Environ Microbiol 13:1454–1466

    Article  CAS  PubMed  Google Scholar 

  • Tomaru Y, Katanozaka N, Nishida K, Shirai Y, Tarutani K, Yamaguchi M, Nagasaki K (2004) 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 

  • Walsh D, Mohr I (2011) Viral subversion of the host protein synthesis machinery. Nat Rev Micro 9:860–875

    Article  CAS  Google Scholar 

  • Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  CAS  PubMed  Google Scholar 

  • Weston AJ, Dunlap WC, Shick JM, Klueter A, Iglic K, Vukelic A, Starcevic A, Ward M, Wells ML, Trick CG, Long PF (2012) A profile of an endosymbiont-enriched fraction of the coral Stylophora pistillata reveals proteins relevant to microbial-host interactions. Mol Cell Proteomics 11(M111):015487

    PubMed  Google Scholar 

  • Weynberg KD, Allen MJ, Ashelford K, Scanlan DJ, Wilson WH (2009) From small hosts come big viruses: the complete genome of a second Ostreococcus tauri virus, OtV-1. Environ Microbiol 11:2821–2839

    Article  CAS  PubMed  Google Scholar 

  • Weynberg KD, Wood-Charlson EM, Suttle CA, van Oppen MJH (2014) Generating viral metagenomes from the coral holobiont. Front Microbiol 5:206

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson WH, Francis I, Ryan K, Davy SK (2001) Temperature induction of viruses in symbiotic dinoflagellates. Aquat Microb Ecol 25:99–102

    Article  Google Scholar 

  • Wilson WH, Dale AL, Davy JE, Davy SK (2005a) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148

    Article  Google Scholar 

  • Wilson WH, Schroeder DC, Allen MJ, Holden MTG, Parkhill J, Barrell BG, Churcher C, Hamlin N, Mungall K, Norbertczak H, Quail MA, Price C, Rabbinowitsch E, Walker D, Craigon M, Roy D, Ghazal P (2005b) Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309:1090–1092

    Article  CAS  PubMed  Google Scholar 

  • Wood-Charlson EM, Weynberg KD, Suttle CA, Roux S, van Oppen MJH (2015) Metagenomic characterization of viral communities in corals: mining biological signal from methodological noise. Environ Microbiol 17:3440–3449

    Article  PubMed  Google Scholar 

  • Yutin N, Koonin EV (2012) Hidden evolutionary complexity of nucleo-cytoplasmic large DNA viruses of eukaryotes. Virol J 9:161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yutin N, Wolf YI, Raoult D, Koonin EV (2009) Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J 6:223

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We acknowledge the technical support from Victor Beltran at the AIMS Symbiont Culture Facility and the scientific and technical assistance of the Australian Microscopy and Microanalysis Research Facility (AMMRF) at the Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, a facility funded by the University and the Western Australian and Australian governments. We acknowledge funding from the Australian Research Council SuperScience Fellowship #FS110200034 to K.D.W. and Future Fellowships #FT100100088 and #FT120100480 to M.v.O and N.S.W., respectively. Research reported in this publication was supported by King Abdullah University of Science and Technology.

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Author notes

  1. Elisha M. Wood-Charlson

    Present address: Center for Microbial Oceanography: Research and Education, University of Hawai‘i at Mānoa, Honolulu, HI, USA

Authors and Affiliations

  1. Australian Institute of Marine Science, PMB #3, Townsville, QLD, 4810, Australia

    Karen D. Weynberg, Patrick Laffy, Nicole S. Webster, Elisha M. Wood-Charlson & Madeleine J. H. van Oppen

  2. Division of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Jeddah, 23955-6900, Saudi Arabia

    Matthew Neave & Christian R. Voolstra

  3. Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Perth, WA, 6009, Australia

    Peta L. Clode

  4. The Oceans Institute, The University of Western Australia, Perth, WA, 6009, Australia

    Peta L. Clode

  5. Biological Resources Imaging Laboratory, University of New South Wales, Sydney, Australia

    Christopher Brownlee

  6. Centre for Marine Bio-Innovation, The University of New South Wales, Sydney, NSW, 2052, Australia

    Rachel A. Levin

  7. Plant Functional Biology and Climate Change Cluster, University of Technology Sydney, Sydney, NSW, Australia

    Rachel A. Levin

  8. School of BioSciences, The University of Melbourne, Parkville, Melbourne, VIC, 3010, Australia

    Madeleine J. H. van Oppen

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  1. Karen D. Weynberg
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Correspondence to Karen D. Weynberg.

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Weynberg, K.D., Neave, M., Clode, P.L. et al. Prevalent and persistent viral infection in cultures of the coral algal endosymbiont Symbiodinium . Coral Reefs 36, 773–784 (2017). https://doi.org/10.1007/s00338-017-1568-7

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