New insights into the genetic diversity of zooxanthellae in Mediterranean anthozoans

Abstract

Symbiotic dinoflagellates of the genus Symbiodinium, also called zooxanthellae, are found in association with a wide diversity of shallow-water anthozoans. The Symbiodinium genus includes numerous lineages, also referred to as clades or phylotypes, as well as a wide diversity of genetic sub-clades and sub-phylotypes. There are few studies characterizing the genetic diversity of zooxanthellae in Mediterranean anthozoans. In this study, we included anthozoans from the Western Mediterranean Sea and by means of internal transcriber (ITS) and large sub-unit (LSU) rRNA markers we corroborate what has been previously identified, demonstrating that phylotype “Temperate A” is very common among host Cnidaria in this basin. Our finding of fixed differences in ITS and LSU markers that correspond to different host taxa, indicate that this clade may comprise several closely-related species. Previous studies have reported the occurrence of Symbiodinium psygmophilum (formerly sub-clade B2) associated with Oculina patagonica and Cladocora caespitosa in the Eastern Mediterranean. Here, we identify this association in O. patagonica from the Western Mediterranean but not in C. caespitosa, suggesting some differences in symbiotic combinations between the Western and Eastern Mediterranean Basins.

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References

  1. Baillie BK, Belda-Baillie CA, Maruyama T (2000) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J Phycol 36:1153–1161

    CAS  Article  Google Scholar 

  2. Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean Acroporid corals. In: Lessios HA, Macintyre IG (eds) Proceedings 8th international coral reef symposium, Vol. 2. Smithsonian Tropical Research Institute, Balboa, Panama, pp 1295–1300

  3. Baker AC, Rowan R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and eastern pacific. In: Lessios HA, Macintyre IG (eds) Proceedings 8th international coral reef symposium, Vol. 2. Smithsonian Tropical Research Institute, Balboa, Panama, pp 1301–1306

  4. Baker AC (1999) The symbiosis ecology of reef-building corals. Ph.D. dissertation. University of Miami, Miami, FL, 120 pp

    Google Scholar 

  5. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  6. Barbrook AC, Visram S, Douglas AE, Christopher JH (2006) Molecular diversity of dinoflagellate symbionts of Cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171

    CAS  PubMed  Article  Google Scholar 

  7. Boudouresque CF (2004) Marine biodiversity in the Mediterranean: status of species, populations and communities. Scientific Reports Port-Cross Natural Park 20:97–146

    Google Scholar 

  8. Coll M, Piroddi C, Steenbeek J, Kaschner K, Lasram FBR, Aguzzi J, Ballesteros E, Bianchi CN, Cobera J, Dailianis T et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One 5:e11842

    PubMed Central  PubMed  Article  Google Scholar 

  9. Coffroth MA, Lasker HR, Diamond ME, Bruenn JA, Birmingham E (1992) DNA fingerprints of a gorgonian coral: a method for detecting clonal structure in a vegetative species. Mar Biol 114:317–325

    CAS  Article  Google Scholar 

  10. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    CAS  PubMed  Article  Google Scholar 

  11. Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172

    CAS  Article  Google Scholar 

  12. Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  13. Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxendorf HA, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and peciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263

    PubMed  Article  Google Scholar 

  14. Forcioli D, Merle P-L, Caligara C, Ciosi M, Muti C, Francour P, Cerrano C, Allemand D (2011) Symbiont diversity is not involved in depth acclimation in the Mediterranean sea whip Eunicella singularis. Mar Ecol Prog Ser 439:57–71

    Article  Google Scholar 

  15. Furla P, Allemand D, Shick JM, Ferrier- Pagès C, Richier S, Plantivaux A, Merle PL, Tambutté (2005) The symbiotic anthozoan: a physiological chimera between algal and animal. Integr Comp Biol 45:595–604

    CAS  PubMed  Article  Google Scholar 

  16. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224

    CAS  PubMed  Article  Google Scholar 

  17. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 5:696–704

    Article  Google Scholar 

  18. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    CAS  PubMed  Article  Google Scholar 

  19. LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    CAS  Article  Google Scholar 

  20. LaJeunesse TC, Loh WKW, vanWoesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern great barrier reef corals relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054

    Article  Google Scholar 

  21. LaJeunesse TC, Thornhill DJ, Cox EF, Stnton FG, Fitt wK, Schmidt W (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603

    Google Scholar 

  22. LaJeunesse TC, Pettay T, Sampayo EM, Phongsuwan N, Brown B, Obura D, Hoegh-Guldberg O, Fitt WK (2010) Special Paper: Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800

    Article  Google Scholar 

  23. LaJeunesse TC, Parkinson J, Reimer JD (2012) A genetic-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidarian. J Phycol 48:1380–1391

    Article  Google Scholar 

  24. Loh WKW, Carter D, Hoegh-Guldberg O (1998) Diversity of zooxanthellae from scleractinian corals of One tree island (The great barrier reef). In: Greenwood JG, Hall NJ (eds) Proceedings of the Australian coral reef society, 75th annual conference. University of Queensland, Brisbane, pp 141–150

    Google Scholar 

  25. Loh WKW, Loi T, Carter D, Hoegh-Guldberg O (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar Ecol Prog Ser 222:97–107

    Article  Google Scholar 

  26. Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, Banin E (2012) Changes in microbial communities in response to a natural pH gradient. ISME J 6:1775–1785

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  27. Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis and evolution. Peerj, e394.

  28. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    CAS  PubMed  Article  Google Scholar 

  29. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Gulberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol 138:1175–1181

    CAS  Article  Google Scholar 

  30. Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol 28:152–168

    CAS  PubMed  Article  Google Scholar 

  31. Rodriguez-Lanetty M, Hoegh-Guldberg O (2003) Symbiont diversity within the widespread scleractinian coral Plesiastrea versipora, across the northwestern Pacific. Mar Biol 143:501–509

    Article  Google Scholar 

  32. Sampayo AM, Dove S, LaJeunesse (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519

    CAS  PubMed  Article  Google Scholar 

  33. Santos SR, Taylor DJ, Coffroth MA (2001) Genetic comparisons of freshly isolated vs. cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. J Phycol 37:866–880

    Article  Google Scholar 

  34. Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth AM (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–11

    CAS  PubMed  Article  Google Scholar 

  35. Savage AM, Goodson MS, Visram S, Trapido-Rosenthal H, Wiedenmann J, Douglas AE (2002) Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar Ecol Prog Ser 244:17–26

    Article  Google Scholar 

  36. Templado J (2014) Future trends of Mediterranean biodiversity. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea: Its history and present challenges, Chapter: 28. Springer, New York

    Google Scholar 

  37. Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium (Dinophyta) lineage. J Phycol 44:1126–1135

    CAS  Article  Google Scholar 

  38. Thornhill DJ, Yiang X, Pettay DT, Zhong SSR (2013) Population genetic dataof a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 2:4499–4515

    Article  Google Scholar 

  39. Trench RK (1993) Microalgal-invertebrate symbioses- a review. Endocytobiosis and Cell Res 9:135–175

    Google Scholar 

  40. Visram S, Wiedenmann J, Douglas AE (2006) Molecular diversity of symbiotic algae of the genus Symbiodinium (Zooxanthellae) in cnidarians of the Mediterranean Sea. J Mar Biol Assoc UK 86:1281–1283

    CAS  Article  Google Scholar 

  41. Weis VM, Reynolds WS, deBoer MD, Krupp DA (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308

    Article  Google Scholar 

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Acknowledgments

The authors want to acknowledge F. Canovas, J. Martinez-Garrido, A. Lerida and A. Addamo for their help in the field with sample collection; R. Garcia-Jimenez and S. Valente for their help and assistance in the molecular laboratory. Dr. Ester Serrão from CCMAR allowed us to carry out the genetic work in her laboratory. M.A. Coffroth for her help with new ideas. We would like also to thanks T. LaJeunesse for his revision on the manuscript and suggestions for improving it. S. Young and K. Nielsen did help us to improve the English grammar and edition. This study was in part performed within the Association of Marine Biology Laboratories Program (ASSEMBLE) under grant agreement no. 227799, carried out at the Center of Marine Sciences (CCMAR) at Algarve University; as well as supported by CUMFISH projects (PTDC/MAR/119363/2010; http://www.ccmar.ualg.pt/cumfish/) funded by Fundacão para Ciência e Tecnologia (Portugal), CGL2011-23306 funded by the Spanish Ministry of Science and Innovation. P. Casado-Amezua is currently supported by an internship from the Alfred Wegener Institute (AWI), Helmholtz Centre for Polar and Marine Research. M. González-Wangüemert is supported by a FCT postdoctoral fellowship (SFRH/BPD/70689/2010).

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Correspondence to Pilar Casado-Amezúa.

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Casado-Amezúa, P., Machordom, A., Bernardo, J. et al. New insights into the genetic diversity of zooxanthellae in Mediterranean anthozoans. Symbiosis 63, 41–46 (2014). https://doi.org/10.1007/s13199-014-0286-y

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Keywords

  • Symbiodinium sp.
  • Genetic characterization
  • Phylotypes “Temperate A” and B
  • Western Mediterranean