Coral Reefs

, Volume 26, Issue 4, pp 867–882 | Cite as

One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera

  • X. PochonEmail author
  • L. Garcia-Cuetos
  • A. C. Baker
  • E. Castella
  • J. Pawlowski


Recent molecular studies of symbiotic dinoflagellates (genus Symbiodinium) from a wide array of invertebrate hosts have revealed exceptional fine-scale symbiont diversity whose distribution among hosts, regions and environments exhibits significant biogeographic, ecological and evolutionary patterns. Here, similar molecular approaches using the internal transcribed spacer-2 (ITS-2) region were applied to investigate cryptic diversity in Symbiodinium inhabiting soritid foraminifera. Approximately 1,000 soritid specimens were collected and examined during a 12-month period over a 40 m depth gradient from a single reef in Guam, Micronesia. Out of 61 ITS-2 types distinguished, 46 were novel. Most types found are specific for soritid hosts, except for three types (C1, C15 and C19) that are common in metazoan hosts. The distribution of these symbionts was compared with the phylotype of their foraminiferal hosts, based on soritid small subunit ribosomal DNA sequences, and three new phylotypes of soritid hosts were identified based on these sequences. Phylogenetic analyses of 645 host-symbiont pairings revealed that most Symbiodinium types associated specifically with a particular foraminiferal host genus or species, and that the genetic diversity of these symbiont types was positively correlated with the genetic diversity found within each of the three host genera. Compared to previous molecular studies of Symbiodinium from other locations worldwide, the diversity reported here is exceptional and suggests that Micronesian coral reefs are home to a remarkably large Symbiodinium assemblage.


Molecular diversity ITS-2 rDNA Soritinae Symbiodinium Symbiosis 



We thank Louisette Zaninetti, Jackie Guiard, José Fahrni, Rob Rowan, Todd C. LaJeunesse, Scott Fay, James Reimer, Tadashi Maruyama, and Luis Pomar. The Swiss National Science Foundation (3100A0-100415 to Jan Pawlowski), the US (National Science Foundation BIO-OCE 0547169 and 0099301 to Andrew C. Baker), the G. & A. Claraz foundation, the E. & L. Schmiedheiny foundation, the Swiss Academy of Sciences (SAS), and the Augustin-Lombard foundation supported this work.


  1. Apprill AM, Gates RD (2006) Recognizing diversity in coral symbiotic dinoflagellate communities. Mol Ecol 16(6):1127–1134CrossRefGoogle Scholar
  2. Baker AC (2003) Flexibility and specificity of coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst 34:661–689CrossRefGoogle Scholar
  3. Baker AC, Romanski AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Mar Ecol Prog Ser 335:237–242CrossRefGoogle Scholar
  4. Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean acroporid corals. Proc 8th Int Coral Reef Symp 2:1295–1300Google Scholar
  5. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741PubMedCrossRefGoogle Scholar
  6. Barbrook AC, Visram S, Douglas AE, Howe CJ (2006) Molecular diversity of dinoflagellate symbionts of cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171PubMedCrossRefGoogle Scholar
  7. Belda-Baillie CA, Sison M, Silvestre V, Villamor K, Monje V, Gomez ED, Baillie BK (1999) Evidence for changing symbiotic algae in juvenile tridacnids. J Exp Mar Biol Ecol 241:207–221CrossRefGoogle Scholar
  8. Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J Phycol 35:1054–1062CrossRefGoogle Scholar
  9. Chen CA, Wang JT, Fang LS, Yang YW (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121CrossRefGoogle Scholar
  10. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  11. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34PubMedCrossRefGoogle Scholar
  12. Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian algal symbiosis. Mar Ecol Prog Ser 222:85–96CrossRefGoogle Scholar
  13. Diekmann OE, Olsen JL, Stam WT, Bak RPM (2003) Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles). Coral Reefs 22:29–33Google Scholar
  14. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  15. Garcia-Cuetos L, Pochon X, Pawlowski J (2006) Molecular evidence for host–symbiont specificity in soritid foraminifera. Protist 156:399–412CrossRefGoogle Scholar
  16. Goulet TL (2006) Most corals may not change their symbionts. Mar Ecol Prog Ser 321:1–7CrossRefGoogle Scholar
  17. Goulet TL (2007) Most scleractinian corals and octocorals host a single symbiotic zooxanthella clade. Mar Ecol Prog Ser 335:243–248CrossRefGoogle Scholar
  18. Guidon S, Gascuel O (2003) A simple, fast and acurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefGoogle Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98Google Scholar
  20. Harris DS, Crandall KA (2000) Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Mol Biol Evol 17:284–291PubMedGoogle Scholar
  21. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  22. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–414CrossRefGoogle Scholar
  23. Karako-Lampert S, Katcoff DJ, Achituv Y, Dubinsky Z, Stambler N (2004) Do clades of symbiotic dinoflagellates in scleractinian corals of the Gulf of Eilat (Red Sea) differ from those of other coral reefs? J Exp Mar Biol Ecol 311:301–314CrossRefGoogle Scholar
  24. LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbiontic dinoflagellates of the genus Symbiodinium using the internal transcribed spacer region: in search of a “species” level marker. J Phycol 37:866–880CrossRefGoogle Scholar
  25. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  26. LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene–Pliocene transition. Mol Biol Evol 22:570–581PubMedCrossRefGoogle Scholar
  27. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–34PubMedCrossRefGoogle Scholar
  28. LaJeunesse TC, Loh WK, Van Woesik 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 48:2046–2054CrossRefGoogle Scholar
  29. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004a) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603Google Scholar
  30. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004b) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161CrossRefGoogle Scholar
  31. Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93PubMedCrossRefGoogle Scholar
  32. Lee JJ (2001) Living sands: symbiosis between foraminifera and algae. Symbiosis 18:489–506Google Scholar
  33. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbiosis shapes growth in reef corals. Science 304:1492–1492PubMedCrossRefGoogle Scholar
  34. Lobban CS, Schefter M, Simpson AGB, Pochon X, Pawlowski J, Foissner W (2002) Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Alveolata, Ciliophora) with zooxanthellae, from Pacific coral reefs. Mar Biol 140:411–423CrossRefGoogle Scholar
  35. Magalon H, Baudry E, Husté A, Adjeroud M, Veuille M (2006) High genetic diversity of the symbiotic dinoflagellates in the coral Pocillopora meandrina from the South Pacific. Mar Biol 148:913–922CrossRefGoogle Scholar
  36. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs (in press)Google Scholar
  37. Pauley G (2003) Marine biodiversity of Guam and the Marianas: overview. Micronesica 35:3–25Google Scholar
  38. Pawlowski J, Holzmann M, Fahrni J, Pochon X, Lee JJ (2001) Molecular identification of algal endosymbionts in large miliolid foraminifera: 2. Dinoflagellates. J Eukaryot Microbiol 48:368–373PubMedCrossRefGoogle Scholar
  39. Pochon X (2006) Diversity, specificity, dynamics, and evolution of the soritid–Symbiodinium symbiosis. PhD thesis, University of Geneva, p 182Google Scholar
  40. Pochon X, Pawlowski J (2006) Evolution of the soritid–Symbiodinium symbiosis: a review. Symbiosis 42:77–88Google Scholar
  41. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078CrossRefGoogle Scholar
  42. Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27CrossRefGoogle Scholar
  43. Pochon X, Montoya JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30PubMedCrossRefGoogle Scholar
  44. Reimer JD, Takishita K, Ono S, Tsukahara J, Maruyama T (2006) Latitudinal and intracolony ITS-rDNA sequence variation in the symbiotic dinoflagellate genus Symbiodinium (Dinophyceae) in Zoanthus sansibaricus (Anthozoa: Hexacorallia). Phycol Res 54:122–132CrossRefGoogle Scholar
  45. Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol 28:152–168PubMedCrossRefGoogle Scholar
  46. Rodriguez-Lanetty M, Chang SJ, Song JI (2003) Specificity of two temperate dinoflagellate–anthozoan associations from the north-western Pacific Ocean. Mar Biol 143:1193–1199CrossRefGoogle Scholar
  47. Rodriguez-Lanetty M, Krupp DA, Weis VM (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
  48. Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs, a review. J Phycol 34:407–417CrossRefGoogle Scholar
  49. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742PubMedCrossRefGoogle Scholar
  50. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral–algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853PubMedCrossRefGoogle Scholar
  51. Rowan R, Knowlton N, Baker AC, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269PubMedCrossRefGoogle Scholar
  52. Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111PubMedCrossRefGoogle Scholar
  53. Santos SR, Kinzie III RA, Sakai K, Coffroth MA (2003) Molecular characterization of nuclear small subunit (18S)-rDNA pseudogenes in a symbiotic dinoflagellate (Symbiodinium, Dinophyta). J Eukaryot Microbiol 50:417–421PubMedCrossRefGoogle Scholar
  54. Santos SR, Shearer TL, Hannes AR, Coffroth MA (2004) Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Mol Ecol 13:459–469PubMedCrossRefGoogle Scholar
  55. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43CrossRefGoogle Scholar
  56. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer, SunderlandGoogle Scholar
  57. Thioulouse J, Chessel D, Dolédec S, Olivier JM (1997) ADE-4: a multivariate analysis and graphical display software. Stat Comput 7:75–83CrossRefGoogle Scholar
  58. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  59. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral–algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722CrossRefGoogle Scholar
  60. Trench RK (1993) Microalgal–invertebrate symbiosis: a review. Endocytobiosis and Cell Research 9:135–175Google Scholar
  61. Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484PubMedCrossRefGoogle Scholar
  62. van Herwerden L, Blair D, Agatsuma T (1999) Intra- and interindividual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: implications for phylogenetic studies. Mol Phylogenet Evol 12:67–73PubMedCrossRefGoogle Scholar
  63. van Oppen MJH, Palstra FP, Piquet AMT, Miller DJ (2001) Patterns of coral dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host–symbiont selectivity. Proc R Soc Lond B Biol Sci 268:1759–1767CrossRefGoogle Scholar
  64. van Oppen MJH, Mioeg JC, Sanchez CA, Fabricius KE (2005a) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the role of geography and the host relationships. Mol Ecol 14:2403–2417PubMedCrossRefGoogle Scholar
  65. van Oppen MJH, Mahiny AJ, Done TJ (2005b) Geographic distribution of zooxanthella groups in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487CrossRefGoogle Scholar
  66. van Oppen MJH, Gates RD (2006) Conservation genetics and resilience of reef-building corals. Mol Ecol 15:3863–3883PubMedCrossRefGoogle Scholar
  67. Wörheide G, Nichols SA, Goldberg J (2004) Intragenomic variation of rDNA internal transcribed spacers in sponges (Phylum Porifera): implications for phylogenetic studies. Mol Phylogenet Evol 33:816–830PubMedCrossRefGoogle Scholar
  68. Zar JH (1999) Biostatistical analysis. Prentice Hall International, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • X. Pochon
    • 1
    • 2
    Email author
  • L. Garcia-Cuetos
    • 1
  • A. C. Baker
    • 3
  • E. Castella
    • 4
  • J. Pawlowski
    • 1
  1. 1.Department of Zoology and Animal Biology, Molecular Systematics GroupUniversity of GenevaGeneva 4Switzerland
  2. 2.Department of Zoology, Hawaii Institute of Marine BiologyUniversity of ManoaKaneoheUSA
  3. 3.Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  4. 4.Laboratory of Ecology and Aquatic BiologyUniversity of GenevaGenevaSwitzerland

Personalised recommendations