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Megaviridae-like particles associated with Symbiodinium spp. from the endemic coral Mussismilia braziliensis

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Abstract

Coral reefs are one of the most dynamic and productive marine ecosystems. The coral holobiont consists of the coral animal and a variety of associated microorganisms that include symbiotic dinoflagellates of the genus Symbiodinium, bacteria, archaea, fungi and viruses. The interactions among these components are crucial for coral health and, consequently, to the coral reef resilience to disturbance. Environmental stressors such as elevated temperature, high irradiance and ultraviolet (UV) radiation can lead to the breakdown of the coral-Symbiodinium symbiosis in a phenomenon known as “coral bleaching”. The present study provides evidence for virus-like particles (VLPs) induced in UV-irradiated Symbiodinium spp. cultures (clades A and C) that were isolated from the coral Mussismilia braziliensis, suggesting a latent viral infection in these strains. Scanning and transmission electron microscopy images of the UV stressed cultures revealed the presence of giant (ca. 450 nm) and small (ca. 40 nm) VLPs. Morphological features link the giant VLPs to the family Megaviridae. Symbiodinium spp. Megaviridae giant viruses and other associated viruses may represent dynamic forces driving and influencing health of the coral holobiont.

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References

  • Andrés G, García-Escudero R, Simón-Mateo C, Viñuela E (1998) African swine fever virus is enveloped by a two-membraned collapsed cisterna derived from the endoplasmic reticulum. J Virol 72:8988–9001

    PubMed  PubMed Central  Google Scholar 

  • Anthony KRN, Kerswell AP (2007) Coral mortality following extreme low tides and high solar radiation. Mar Biol 151:1623–1631

    Article  Google Scholar 

  • Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proceedings of the National Academy of Sciences of the United States of America 108:17486-17491

    Article  CAS  Google Scholar 

  • Bettarel Y, Bouvier T, Nguyen HK, Thu PT (2015) The versatile nature of coral-associated viruses. Environ Microbiol 17:3433–3439

    Article  PubMed  Google Scholar 

  • Bettarel Y, Thuy NT, Huy TQ, Hoang PK, Bouvier T (2013) Observation of virus-like particles in thin sections of the bleaching scleractinian coral Acropora cytherea. J Mar Biol Assoc U K 93:909–912

    Article  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16(Suppl 1):S129–S138

    Article  Google Scholar 

  • Brüwer JD, Agrawal S, Liew YJ, Aranda M, Voolstra CR (2017) Association of coral algal symbionts with a diverse viral community responsive to heat shock. BMC Microbiol 17:174

    Article  PubMed  PubMed Central  Google Scholar 

  • Campos RK, Boratto PV, Assis FL, Aguiar ER, Silva LC, Albarnaz JD, Dornas FP, Trindade GS, Ferreira PP, Marques JT, Robert C, Raoult D, Kroon EG, La Scola B, Abrahão JS (2014) Samba virus: a novel Mimivirus from a giant rain forest, the Brazilian Amazon. Virol J 11:95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro AP, Araújo SDJR, Reis AM, Moura RL, Francini-Filho RB, Pappas GJR, Rodrigues TB, Thompson FL, Krüger RH (2010) Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from Eastern Brazil. Micro Eco 59:658–667

    Article  Google Scholar 

  • Castro CB, Pires DO (1999) A bleaching event on a Brazilian coral reef. Braz J Oceanogr 47:87–90

    Article  Google Scholar 

  • Cervino JM, Hayes R, Goreau TJ, Smith GW (2004) Zooxanthellae regulation in yellow blotch/band and other coral diseases contrasted with temperature related bleaching: In situ destruction vs expulsion. Symbiosis 37:6–85

    Google Scholar 

  • Claverie JM, Grzela R, Lartigue A, Bernadac A, Nitsche S, Vacelet J, Ogata H, Abergel C (2009) Mimivirus and Mimiviridae: Giant viruses with an increasing number of potential hosts, including corals and sponges. J Invertebr Pathol 101:172–180

    Article  CAS  PubMed  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 7:00127

    Article  Google Scholar 

  • Correa AMS, Welsh RM, Vega Thurber RL (2013) Unique nucleocytoplasmic dsDNA and +ssRNA viruses are associated with the dinoflagellate endosymbionts of corals. ISME J 7:13–27

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Davy SKS, Burchett G, Dale AL, Davies P, Davy JE, Muncke C, Hoegh-Guldberg O, Wilson WH (2006) Viruses: agents of coral disease? Diseases of Aquatic Organisms 69:101–110

    Article  CAS  PubMed  Google Scholar 

  • Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin SA, Thurber RV, Willis BL, Azam F, Knowlton N, Rohwer F (2008) Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 3:e1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernando SC, Wang J, Sparling K, Garcia GD, Francini-Filho RB, de Moura RL, Paranhos R, Thompson FL, Thompson JR (2014) Microbiota of the major South Atlantic reef building coral Mussismilia. Micro Eco 69:267–280

    Article  PubMed  Google Scholar 

  • Fischer MG, Suttle CA (2011) A virophage at the origin of large DNA transposons. Science 332:231–234

    Article  CAS  PubMed  Google Scholar 

  • Francini-Filho RB, Moura RL, Thompson FL, Reis RM, Kaufman L, Kikuchi RKP, Leão ZMAN (2008) Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil). Mar Pollut Bull 56:1008–1014

    Article  CAS  PubMed  Google Scholar 

  • Francini-Filho RB, Reis R, Meirelles P, Moura R, Thompson F, Kikuchi R, Kaufman L (2010) Seasonal prevalence of white plague like disease on the endemic Brazilian reef coral Mussismilia braziliensis. Lat Am J Aquat Res 38:292–296

    Article  Google Scholar 

  • Garcia GD, Gregoracci GB, Santos E de O, Meirelles PM, Silva GGZ, Edwards R, Sawabe T, Gotoh K, Nakamura S, Iida T, de Moura RL, Thompson FL (2013) Metagenomic analysis of healthy and white plague-affected Mussismilia braziliensis corals. Microb Ecol 65:1076–1086

    Article  PubMed  Google Scholar 

  • Garcia GD, Santos Ede O, Sousa GV, Zingali RB, Thompson CC, Thompson FL (2016) Metaproteomics reveals metabolic transitions between healthy and diseased stony coral Mussismilia braziliensis. Mol Ecol 25:4632–4644

    Article  CAS  PubMed  Google Scholar 

  • Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838

    Article  Google Scholar 

  • Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17

    Article  Google Scholar 

  • Goulet TL, Coffroth MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23:465–472

    Google Scholar 

  • Greiner T, Frohns F, Kang M, Van Etten JL, Käsmann A, Moroni A, Hertel B, Thiel G (2009) Chlorella viruses prevent multiple infections by depolarizing the host membranes. J Gen Virol 90:2033–2039

    Article  CAS  PubMed  Google Scholar 

  • Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. P  Natl Acad Sci USA 96:2192–2197

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O (2004) Coral reefs in a century of rapid environmental change. Symbiosis 37:1–31

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Kendall A, McDonald M, Bian W, Bowles T, Baumgarten SC, Shi J, Stewart PL, Bullitt E, Gore D, Irving TC, Havens WM, S a G, Wall JS, Stubbs G (2008) Structure of flexible filamentous plant viruses. J Virol 82:9546–9554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knowlton N, Rohwer F (2003) Microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62

  • La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E (2008) The virophage as a unique parasite of the giant Mimivirus. Nature 455:100–104

    Article  CAS  PubMed  Google Scholar 

  • Lawrence SA, Davy JE, Wilson WH, Hoegh-Guldberg O, Davy SK (2014a) Porites white patch syndrome: associated viruses and disease physiology. Coral Reefs 34:249–257

    Article  Google Scholar 

  • Lawrence SA, Wilson WH, Davy JE, Davy SK (2014b) Latent virus-like infections are present in a diverse range of Symbiodinium spp. (Dinophyta). J Phycol 50:984–997

    Article  PubMed  Google Scholar 

  • Lawrence SA, Floge SA, Davy JE, Davy SK, Wilson WH (2017) Exploratory analysis of Symbiodinium transcriptomes reveals potential latent infection by large dsDNA viruses. Environ Microbiol 19(10):3909–3919

    Article  CAS  PubMed  Google Scholar 

  • Leão ZMAN, Kikuchi RKP (2005) A relic coral fauna threatened by global changes and human activities, Eastern Brazil. Mar Pollut Bull 51:599–611

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283

    Article  CAS  Google Scholar 

  • Levin RA, Voolstra CR, Weynberg KD, and van Open, MJH (2017). Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J 11(3):808-812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Littman R, Willis BL, Bourne DG (2011) Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Rep 3:651–660

    Article  CAS  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 

  • Margulis L (1991) Symbiogenesis and symbionticism. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press, Cambridge, pp 1–24

    Google Scholar 

  • Marhaver KL, Edwards RA, Rohwer F (2008) Viral communities associated with healthy and bleaching corals. Environ Microbiol 10:2277–2286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minarovits J (2006) Epigenotypes of latent herpesvirus genomes. Curr Top Microbiol Immunol 310:61–80

    CAS  PubMed  Google Scholar 

  • Mindell DP (1992) Phylogenetic consequences of symbioses: Eukarya and Eubacteria are not monophyletic taxa. BioSystems 27:53–62

    Article  CAS  PubMed  Google Scholar 

  • Mutsafi Y, Shimoni E, Shimon A, Minsky A (2013) Membrane assembly during the infection cycle of the giant Mimivirus. PLoS Pathogens 9:e1003367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen-Kim H, Bouvier T, Bouvier C, Doan-Nhu H, Nguyen-Ngoc L, Rochelle-Newall E, Baudoux AC, Desnues C, Reynaud S, Ferrier-Pages C, Bettarel Y (2014) High occurrence of viruses in the mucus layer of scleractinian corals. Environ Microbiol Rep 66:675–682

    Article  Google Scholar 

  • Patten NL, Harrison PL, Mitchell JG (2008) Prevalence of virus-like particles within a staghorn scleractinian coral (Acropora muricata) from the Great Barrier Reef. Coral Reefs 27:569–580

    Article  Google Scholar 

  • Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27

    Article  Google Scholar 

  • Reis AMM, Araújo SD, Moura RL, Francini-Filho RB, Pappas G, Coelho AMA, Krüger RH, Thompson FL (2009) Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis. J Appl Microbiol 106:1378–1387

    Article  CAS  PubMed  Google Scholar 

  • Riegl B, Bruckner A, Coles SL, Renaud P, Dodge RE (2009) Coral reefs: Threats and conservation in an era of global change. Ann N Y Acad Sci 1162:136–186

    Article  CAS  PubMed  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, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  PubMed  Google Scholar 

  • Rowe JM, Dunlap JR, Gobler CJ, Anderson OR, Gastrich MD, Wilhelm SW (2008) Isolation of a non-phage-like lytic virus infecting Aureococcus anophagefferens. J Phycol 44:71–76

    Article  PubMed  Google Scholar 

  • Sampayo EM, Ridgway T, Franceschinis L, Roff G, Hoegh-Guldberg O, Dove S (2016) Coral symbioses under prolonged environmental change: living near tolerance range limits. Sci Rep 6:36271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santini S, Jeudy S, Bartoli J, Poirot O, Lescot M, Abergel C, Barbe V, Wommack KE, Noordeloos AAM, Brussaard CPD, Claverie JM (2013) Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. P Natl Acad Sci USA 110:10800–10805

    Article  CAS  Google Scholar 

  • Silva-Lima AW, Walter JM, Garcia GD, Ramires N, Ank G, Meirelles PM, Nobrega AF, Siva-Neto ID, Moura RL, Salomon PS, Thompson CC, Thompson FL (2015) Multiple Symbiodinium Strains Are Hosted by the Brazilian Endemic Corals Mussismilia spp. Microb Ecol 70:301–310

    Article  PubMed  Google Scholar 

  • Silveira CB, Gregoracci GB, Coutinho FH, Silva GGZ, Haggerty JM, de Oliveira LS, Cabral AS, Rezende CE, Thompson CC, Francini-Filho RB, Edwards RA, Dinsdale EA, Thompson FL (2017) Bacterial community associated with the reef coral Mussismilia braziliensis’s momentum boundary layer over a diel cycle. Front Microbiol 8:784

  • Soffer N, Brandt ME, Correa AMS, Smith TB, Thurber RV (2014) Potential role of viruses in white plague coral disease. ISME J 8:271–283

    Article  CAS  PubMed  Google Scholar 

  • Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D (2007) Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS One 2:e328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sweet MJ, Bythell MT (2016) The role of viruses in coral health and disease. J Invertebr Pathol 147:136–144

    Article  PubMed  Google Scholar 

  • Thompson JR, Rivera HE, Closek CJ, Medina M (2014) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4:176

    PubMed  Google Scholar 

  • Thurber RLV, Correa AMS (2011) Viruses of reef-building scleractinian corals. J Exp Mar Biol Ecol 408:102–113

    Article  Google Scholar 

  • Thurber RLV, Barott KL, Hall D, Liu H, Rodriguez-Mueller B, Desnues C, Edwards RA, Haynes M, Angly FE, Wegley L, Rohwer FL (2008) Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. P Natl Acad Sci USA 105:18413–18418

  • Thurber RV, Payet JP, Thurber AR, Correa AMS (2017) Virus–host interactions and their roles in coral reef health and disease. Nat Rev Microbiol 15:205–216

    Article  CAS  PubMed  Google Scholar 

  • van Oppen MJH, Leong JA, Gates RD (2009) Coral-virus interactions: A double-edged sword? Symbiosis 47:1–8

    Article  Google Scholar 

  • van Oppen MJH, Lough JM (2009) Introduction: Coral Bleaching - Patterns, Processes, Causes and Consequences. In: van Oppen MJH, Lough JM (eds) Coral Bleaching. Ecological Studies, vol 205. Springer, Berlin, Heidelberg, pp 1-5

  • Veesler D, Cambillau CA (2011) A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol Mol Biol Rev 75:423–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weynberg KD, Levin RA, Neave MJ, Clode PL, Voolstra CR, Brownlee C, Laffy PW, Webster NS, Wood-Charlson EM, van Oppen MJH (2017) Prevalent and persistent viral infection in cultures of the coral algal endosymbiont, Symbiodinium. Coral Reefs 36(3):773-784

    Article  Google Scholar 

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

    Article  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 

  • 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 

  • Wooldridge SA (2013) Breakdown of the coral-algae symbiosis: Towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences 10:1647–1658

    Article  Google Scholar 

  • Zhou J, Huang H, Beardall J, Gao K (2016) Effect of UV radiation on the expulsion of Symbiodinium from the coral Pocillopora damicornis. J Photochem Photobiol B 166:12–17

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are thankful to Dr. Paulo Iiboshi Hargreaves and Dr. Glaucia Ank for their assistance with Symbiodinium spp. cultures. We greatly appreciate the helpful discussion, corrections and insightful comments provided by Lilian Caesar, Sheree Yau and two anonymous referees. This work was made possible by grants from the Brazilian Research Councils Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grants 305347/2016-0 and 407297/2013-8 to PSS), and Rio de Janeiro State Research Council Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

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  1. Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ, Rio de Janeiro, Brazil

    Luiz Felipe Benites, Arthur Weiss Silva-Lima & Paulo Sergio Salomon

  2. Programa de Pós-Graduação em Biodiversidade e Biologia Evolutiva, UFRJ, Rio de Janeiro, Brazil

    Luiz Felipe Benites, Arthur Weiss Silva-Lima & Paulo Sergio Salomon

  3. Departamento de Zoologia, Instituto de Biologia, UFRJ, Rio de Janeiro, Brazil

    Inácio Domingos da Silva-Neto

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  1. Luiz Felipe Benites
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Correspondence to Paulo Sergio Salomon.

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Benites, L.F., Silva-Lima, A.W., da Silva-Neto, I.D. et al. Megaviridae-like particles associated with Symbiodinium spp. from the endemic coral Mussismilia braziliensis. Symbiosis 76, 303–311 (2018). https://doi.org/10.1007/s13199-018-0567-y

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