Skip to main content
SpringerLink
Log in

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)

  • Note
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 352:338–342

    Article  CAS  PubMed  Google Scholar 

  • Bogdan C, Nathan C (1993) Modulation of macrophage function by transforming growth factor beta, interleukin-4, and interleukin-10. Ann N Y Acad Sci 685:713–739

    Article  CAS  PubMed  Google Scholar 

  • Buckley KM, Rast JP (2012) Dynamic evolution of toll-like receptor multigene families in echinoderms. Front Immunol 3:136

    Article  PubMed  PubMed Central  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian–dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 38:525–537

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (2003) Coral bleaching—how and why? Mar Pollut Bull 46:385–392

    Article  CAS  PubMed  Google Scholar 

  • Franchini A, Malagoli D, Ottaviani E (2006) Cytokines and invertebrates: TGF-beta and PDGF. Curr Pharm Des 12:3025–3031

    Article  CAS  PubMed  Google Scholar 

  • 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 62:17–28

    Article  CAS  PubMed  Google Scholar 

  • 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 30:167–176

    Article  CAS  PubMed  Google Scholar 

  • 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 122:695–705

    Article  CAS  PubMed  Google Scholar 

  • 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 543:373–377

    Article  CAS  PubMed  Google Scholar 

  • 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:e88615

    Article  PubMed  PubMed Central  Google Scholar 

  • Kitchen SA, Crowder CM, Poole AZ, Weis VM, Meyer E (2015) De novo assembly and characterization of four anthozoan (Phylum Cnidaria) transcriptomes. G3 (Bethesda) 5:2441–2452

    Article  Google Scholar 

  • Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791

    Article  CAS  PubMed  Google Scholar 

  • McFall-Ngai M (2008) Are biologists in ‘future shock’? Symbiosis integrates biology across domains. Nat Rev Microbiol 6:789–792

    Article  CAS  PubMed  Google Scholar 

  • Messier-Solek C, Buckley KM, Rast JP (2010) Highly diversified innate receptor systems and new forms of animal immunity. Semin Immunol 22:39–47

    Article  CAS  PubMed  Google Scholar 

  • 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:R59

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 222:181–202

    Article  CAS  Google Scholar 

  • Normile D (2016) El Nino’s warmth devastating reefs worldwide. Science 352:15–16

    Article  CAS  PubMed  Google Scholar 

  • 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 90:2905–2909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e24152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 275:97–102

    Article  CAS  Google Scholar 

  • Rodriguez-Lanetty M, Phillips WS, Weis VM (2006) Transcriptome analysis of a cnidarian–dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7:23

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 685:488–500

    Article  CAS  PubMed  Google Scholar 

  • 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 90:6004–6008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuel G, Miller D, Saint R (2001) Conservation of a DPP/BMP signaling pathway in the nonbilateral cnidarian Acropora millepora. Evol Dev 3:241–250

    Article  CAS  PubMed  Google Scholar 

  • Schnitzler CE, Weis VM (2010) Coral larvae exhibit few measurable transcriptional changes during the onset of coral–dinoflagellate endosymbiosis. Mar Genomics 3:107–116

    Article  PubMed  Google Scholar 

  • Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196:70–79

    Article  CAS  PubMed  Google Scholar 

  • 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 476:320–323

    Article  CAS  PubMed  Google Scholar 

  • 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 466:720–726

    Article  CAS  PubMed  PubMed Central  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 

  • Yellowlees D, Rees TA, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  PubMed  Google Scholar 

  • 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) 11:260–269

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, Oregon State University, Corvallis, OR, USA

    Jérémy Berthelier, Angela Z. Poole, Virginia M. Weis & Olivier Detournay

  2. Physiology and Biotechnology of Algae Laboratory, Ifremer, 44311, Nantes, France

    Jérémy Berthelier

  3. Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL, USA

    Christine E. Schnitzler

  4. Department of Biology, University of Florida, Gainesville, FL, USA

    Christine E. Schnitzler

  5. Center for Microbial Oceanography, University of Hawai‘i, Mānoa, HI, USA

    Elisha M. Wood-Charlson

  6. Department of Biology, Western Oregon University, Monmouth, OR, USA

    Angela Z. Poole

  7. Planktovie sas, 13190, Allauch, France

    Olivier Detournay

Authors
  1. Jérémy Berthelier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christine E. Schnitzler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elisha M. Wood-Charlson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Angela Z. Poole
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Virginia M. Weis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Olivier Detournay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jérémy Berthelier.

Additional information

Communicated by Biology Editor Dr. Line K. Bay

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 479 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berthelier, J., Schnitzler, C.E., Wood-Charlson, E.M. et al. 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). Coral Reefs 36, 1263–1268 (2017). https://doi.org/10.1007/s00338-017-1621-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-017-1621-6

Keywords

Search

Navigation