Skip to main content

Establishment of a model for chemoattraction of Symbiodinium and characterization of chemotactic compounds in Acropora tenuis

Abstract

Corals harbor symbiotic dinoflagellates, Symbiodinium spp., acquired from surrounding environments. Because Symbiodinium are present at low densities in the water column, corals may attract these symbionts using chemotactic compounds. To examine whether corals contain chemotactic compounds, we established an assay to measure the chemotactic activity for Symbiodinium using an extract of the coral Acropora tenuis, a major reef-building coral in Japan. Our assay revealed that Symbiodinium strain NBRC102920 (clade A), which is taken up by juvenile A. tenuis polyps, is attracted to crude A. tenuis extracts. We found that the chemotactic compounds are water-soluble, heat-labile macromolecules and that the chemotactic activity was inhibited by N-acetyl-d-glucosamine (GlcNAc). We separated the GlcNAc-binding fraction (Fr-ActL) and identified it as the most plausible candidate for the chemoattractant, since the chemotactic activity of the crude A. tenuis extract appeared to be mainly attributable to the activity of Fr-ActL and was also inhibited by the addition of GlcNAc. These results indicate that chemoattraction is mediated via the binding of Symbiodinium to Fr-ActL.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. 1.

    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 

  2. 2.

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

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571

    Article  Google Scholar 

  4. 4.

    Yamashita H, Suzuki G, Hayashibara T, Koike K (2013) Acropora recruits harbor “rare” Symbiodinium in the environmental pool. Coral Reefs 32:355–366

    Article  Google Scholar 

  5. 5.

    Fitt WK, Chang SS, Trench RK (1981) Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium (=Gymnodinium) microadriaticum (Freudenthal) in culture. Bull Mar Sci 31:436–443

    Google Scholar 

  6. 6.

    Fitt WK (1984) The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and molluscs with zooxanthellae. Mar Biol 81:9–17

    Article  Google Scholar 

  7. 7.

    Pasternak Z, Bachar A, Abelson A, Achituv Y (2004) Initiation of symbiosis between the soft coral Heteroxenia fuscescens and its zooxanthellae. Mar Ecol Prog Ser 279:113–116

    Article  Google Scholar 

  8. 8.

    Yamashita H, Suzuki G, Kai S, Hayashibara T, Koike K (2014) Establishment of coral–algal symbiosis requires attraction and selection. PLoS One 9:e97003

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Fitt WK (1985) Chemosensory responses of the symbiotic dinoflagellate Symbiodinium microadriaticum (Dinophyceae). J Phycol 21:62–67

    Article  Google Scholar 

  10. 10.

    Sjoblad RD, Chet I, Mitchell R (1978) Quantitative assay for algal chemotaxis. Appl Environ Microbiol 36:847–850

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Mar Ecol Prog Ser 256:87–97

    CAS  Article  Google Scholar 

  12. 12.

    Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLW amide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21:127–129

    Google Scholar 

  13. 13.

    Yuyama I, Hayakawa H, Endo H, Iwao K, Takeyama H, Maruyama T, Watanabe T (2005) Identification of symbiotically expressed coral mRNAs using a model infection system. Biochem Biophys Res Commun 336:793–798

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Kuniya N, Jimbo M, Tanimoto F, Yamashita H, Koike K, Harii S, Nakano N, Iwao K, Yasumoto K, Watabe S (2015) Possible involvement of tachylectin-2-like lectin from Acropora tenuis in the process of Symbiodinium acquisition. Fish Sci 81:473–483

    CAS  Article  Google Scholar 

  15. 15.

    Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lajeunesse TC (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blaank. Eur J Phycol 50:155–172

    Article  Google Scholar 

  16. 16.

    Jimbo M, Yoshida T, Koike K, Koike K, Sakai R, Muramoto K, Kamiya H (2000) The d-galactose-binding lectin of the octocoral Sinularia lochmodes: characterization and possible relationship to the symbiotic dinoflagellates. Comp Biochem Physiol B 125:227–236

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Laemmli UK (1970) Cleavage of structural proteins during the assembly on the head of bacteriophage T4. Nature 277:680–685

    Article  Google Scholar 

  18. 18.

    Yoshida M, Murata M, Inaba K, Morisawa M (2002) A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc Natl Acad Sci USA 99:14831–14836

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Miyazaki S, Ichiba T, Reimer JD, Tanaka J (2014) Chemoattraction of the pearlfish Encheliophis vermicularis to the sea cucumber Holothuria leucospilota. Chemoecology 24:121–126

    CAS  Article  Google Scholar 

  20. 20.

    Hagedron M, Carter V, Zuchowicz N, Phillips M, Penfield C, Shamenek B, Vallen EA, Kleinhans FW, Peterson K, White M, Yancey PH (2015) Trehalose is a chemical attractant in the establishment of coral symbiosis. PLoS One 10:e0117087

    Article  Google Scholar 

  21. 21.

    Miller RL, Vogt R (1996) An N-terminal partial sequence of the 13 kDa Pycnopodia helianthoides sperm chemoattractant “startrak” possesses sperm-attracting activity. J Exp Biol 199:311–318

    CAS  PubMed  Google Scholar 

  22. 22.

    Lin KL, Wang JT, Fang LS (2000) Participation of glycoproteins on zooxanthellal cell walls in the establishment of a symbiotic relationship with the sea anemone, Aiptasia pulchella. Zool Stud 39:172–178

    CAS  Google Scholar 

  23. 23.

    Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1993

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Kvenneforts ECE, Leggat W, Kerr CC, Ainsworth TD, Hoegh-Guldberg O, Barnes AC (2010) Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev Comp Immunol 34:1219–1229

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Hiroshi Yamashita for useful advice on the preparation of this manuscript. This work was supported by a Grant-in-Aid for Scientific Research (C) from the Ministry of Education, Culture, Sports, Science and Technology of Japan to MJ [22580228] and partially by a grant-in-aid from The Mikimoto Fund for Marine Ecology, Japan.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mitsuru Jimbo.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Takeuchi, R., Jimbo, M., Tanimoto, F. et al. Establishment of a model for chemoattraction of Symbiodinium and characterization of chemotactic compounds in Acropora tenuis . Fish Sci 83, 479–487 (2017). https://doi.org/10.1007/s12562-017-1069-1

Download citation

Keywords

  • Acropora tenuis
  • Coral
  • Symbiodinium
  • Chemoattraction
  • Lectin