Coral Reefs

, Volume 36, Issue 4, pp 1263–1268 | Cite as

Implication of the host TGFβ pathway in the onset of symbiosis between larvae of the coral Fungia scutaria and the dinoflagellate Symbiodinium sp. (clade C1f)

  • Jérémy BerthelierEmail author
  • Christine E. Schnitzler
  • Elisha M. Wood-Charlson
  • Angela Z. Poole
  • Virginia M. Weis
  • Olivier Detournay


Dinoflagellate–cnidarian associations form both the trophic and structural foundation of coral-reef ecosystems. Previous studies have highlighted the role of host innate immunity in regulation of these partnerships. This study reveals the presence of a transforming growth factor beta (TGFβ) in the coral Fungia scutaria that clusters with TGFβ sensu stricto (ss) from other animals. In functional studies of F. scutaria larvae, we show that (1) TGFβ ss mRNA is expressed during early stages of development prior to the onset of symbiosis; (2) apparent interference of the TGFβ pathway impairs the onset of symbiosis; and (3) this effect is associated with an increase of cytotoxic nitric oxide secretion, an immune response. This work highlights the importance of the TGFβ pathway in early life-history stages of corals by suggesting that its inhibition impacts the onset of symbiosis.


Transforming growth factor beta Cnidarian Coral bleaching Dinoflagellate Symbiodinium Symbiosis 



We thank Jennifer Matthews, Ashley Sproles, Mary Hagedorn, Virginia L. Carter, and Ruth Gates for providing assistance in the field, equipment, and laboratory space. This is Hawaii Institute of Marine Biology contribution #1476. This work has been supported by National Science Foundation Grants to VMW (IOB0542452 and IOB0919073). The 2014 field trip was financed by crowdfunding support to the Coral Guardian NGO foundation. We thank Eric Henry and Eric Rottinger for their help on the redaction as well as Benoit Miel-Istria, Sandrine Convertino, Marie-Christine Rocci, Cristiana Bontemps, and Mariella Coste.

Supplementary material

338_2017_1621_MOESM1_ESM.pdf (480 kb)
Supplementary material 1 (PDF 479 kb)


  1. Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:338–342CrossRefPubMedGoogle Scholar
  2. Bogdan C, Nathan C (1993) Modulation of macrophage function by transforming growth factor beta, interleukin-4, and interleukin-10. Ann N Y Acad Sci 685:713–739CrossRefPubMedGoogle Scholar
  3. Buckley KM, Rast JP (2012) Dynamic evolution of toll-like receptor multigene families in echinoderms. Front Immunol 3:136CrossRefPubMedPubMedCentralGoogle Scholar
  4. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian–dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261CrossRefPubMedPubMedCentralGoogle Scholar
  5. Detournay O, Schnitzler CE, Poole A, Weis VM (2012) Regulation of cnidarian–dinoflagellate mutualisms: evidence that activation of a host TGFbeta innate immune pathway promotes tolerance of the symbiont. Dev Comp Immunol 38:525–537CrossRefPubMedGoogle Scholar
  6. Douglas AE (2003) Coral bleaching—how and why? Mar Pollut Bull 46:385–392CrossRefPubMedGoogle Scholar
  7. Franchini A, Malagoli D, Ottaviani E (2006) Cytokines and invertebrates: TGF-beta and PDGF. Curr Pharm Des 12:3025–3031CrossRefPubMedGoogle Scholar
  8. Fuess LE, Pinzomicronn CJ, Weil E, Mydlarz LD (2016) Associations between transcriptional changes and protein phenotypes provide insights into immune regulation in corals. Dev Comp Immunol 62:17–28CrossRefPubMedGoogle Scholar
  9. Hamada M, Shoguchi E, Shinzato C, Kawashima T, Miller DJ, Satoh N (2013) The complex NOD-like receptor repertoire of the coral Acropora digitifera includes novel domain combinations. Mol Biol Evol 30:167–176CrossRefPubMedGoogle Scholar
  10. Herpin A, Lelong C, Becker T, Rosa FM, Favrel P, Cunningham C (2005) Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria. Mech Dev 122:695–705CrossRefPubMedGoogle Scholar
  11. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefPubMedGoogle Scholar
  12. Karako-Lampert S, Zoccola D, Salmon-Divon M, Katzenellenbogen M, Tambutte S, Bertucci A, Hoegh-Guldberg O, Deleury E, Allemand D, Levy O (2014) Transcriptome analysis of the scleractinian coral Stylophora pistillata. PLoS One 9:e88615CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kitchen SA, Crowder CM, Poole AZ, Weis VM, Meyer E (2015) De novo assembly and characterization of four anthozoan (Phylum Cnidaria) transcriptomes. G3 (Bethesda) 5:2441–2452CrossRefGoogle Scholar
  14. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791CrossRefPubMedGoogle Scholar
  15. McFall-Ngai M (2008) Are biologists in ‘future shock’? Symbiosis integrates biology across domains. Nat Rev Microbiol 6:789–792CrossRefPubMedGoogle Scholar
  16. Messier-Solek C, Buckley KM, Rast JP (2010) Highly diversified innate receptor systems and new forms of animal immunity. Semin Immunol 22:39–47CrossRefPubMedGoogle Scholar
  17. Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TC (2007) The innate immune repertoire in cnidaria—ancestral complexity and stochastic gene loss. Genome Biol 8:R59CrossRefPubMedPubMedCentralGoogle Scholar
  18. Muscatine L, Falkowski P, Porter J, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light-adapted and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B Biol Sci 222:181–202CrossRefGoogle Scholar
  19. Normile D (2016) El Nino’s warmth devastating reefs worldwide. Science 352:15–16CrossRefPubMedGoogle Scholar
  20. Padgett RW, Wozney JM, Gelbart WM (1993) Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci USA 90:2905–2909CrossRefPubMedPubMedCentralGoogle Scholar
  21. Pang K, Ryan JF, Baxevanis AD, Martindale MQ (2011) Evolution of the TGF-beta signaling pathway and its potential role in the ctenophore Mnemiopsis leidyi. PLoS One 6:e24152CrossRefPubMedPubMedCentralGoogle Scholar
  22. Rodriguez-Lanetty M, Krupp DA, Weis V (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar Ecol Prog Ser 275:97–102CrossRefGoogle Scholar
  23. Rodriguez-Lanetty M, Phillips WS, Weis VM (2006) Transcriptome analysis of a cnidarian–dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7:23CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ruscetti F, Varesio L, Ochoa A, Ortaldo J (1993) Pleiotropic effects of transforming growth factor-beta on cells of the immune system. Ann N Y Acad Sci 685:488–500CrossRefPubMedGoogle Scholar
  25. Sampath TK, Rashka KE, Doctor JS, Tucker RF, Hoffmann FM (1993) Drosophila transforming growth factor beta superfamily proteins induce endochondral bone formation in mammals. Proc Natl Acad Sci USA 90:6004–6008CrossRefPubMedPubMedCentralGoogle Scholar
  26. Samuel G, Miller D, Saint R (2001) Conservation of a DPP/BMP signaling pathway in the nonbilateral cnidarian Acropora millepora. Evol Dev 3:241–250CrossRefPubMedGoogle Scholar
  27. Schnitzler CE, Weis VM (2010) Coral larvae exhibit few measurable transcriptional changes during the onset of coral–dinoflagellate endosymbiosis. Mar Genomics 3:107–116CrossRefPubMedGoogle Scholar
  28. Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196:70–79CrossRefPubMedGoogle Scholar
  29. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–323CrossRefPubMedGoogle Scholar
  30. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726CrossRefPubMedPubMedCentralGoogle Scholar
  31. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066CrossRefPubMedGoogle Scholar
  32. Yellowlees D, Rees TA, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694CrossRefPubMedGoogle Scholar
  33. Zoccola D, Moya A, Beranger GE, Tambutte E, Allemand D, Carle GF, Tambutte S (2009) Specific expression of BMP2/4 ortholog in biomineralizing tissues of corals and action on mouse BMP receptor. Mar Biotechnol (NY) 11:260–269CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Integrative BiologyOregon State UniversityCorvallisUSA
  2. 2.Physiology and Biotechnology of Algae LaboratoryIfremerNantesFrance
  3. 3.Whitney Laboratory for Marine BioscienceUniversity of FloridaSt. AugustineUSA
  4. 4.Department of BiologyUniversity of FloridaGainesvilleUSA
  5. 5.Center for Microbial OceanographyUniversity of Hawai‘iMānoaUSA
  6. 6.Department of BiologyWestern Oregon UniversityMonmouthUSA
  7. 7.Planktovie sasAllauchFrance

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