Coral Reefs

, Volume 31, Issue 1, pp 157–167

Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai‘i and Florida

  • M. Takabayashi
  • L. M. Adams
  • X. Pochon
  • R. D. Gates
Report

Abstract

Marine dinoflagellates in the genus Symbiodinium are primarily known for their symbiotic associations with invertebrates and protists, although they are also found free-living in nanoplankton and microphytobenthic communities. Free-living Symbiodinium are necessary for hosts that must acquire their symbionts anew each generation and for the possible reestablishment of endosymbiosis in bleached adults. The diversity and ecology of free-living Symbiodinium are not well studied by comparison with their endosymbiotic counterparts, and as a result, our understanding of the linkages between free-living and endosymbiotic Symbiodinium is poor. Here, we begin to address this knowledge gap by describing the genetic diversity of Symbiodinium in the surface water and reef sediments of Hawai‘i and Florida using Symbiodinium-specific primers for the hypervariable region of the chloroplast 23S domain V (cp23S-HVR). In total, 29 Symbiodinium sequence types were detected, 16 of which were novel. The majority of Symbiodinium sequence types in free-living environments belonged to clades A and B, but smaller numbers of sequence types belonging to clades C, D, and G were also detected. The majority of sequences recovered from Hawai‘i belonged to clades A and C and those from Florida to clade B. Such distribution patterns are consistent with the endosymbiotic diversity previously reported for these two regions. The ancestral sequence types in each clade were typically recovered from surface water and sediments both in Hawai‘i and Florida and have been previously reported as endosymbionts of a range of invertebrates, suggesting that these types have the capacity to exploit a range of very different habitats. More derived sequence types in clades A, B, C, and G were not recovered here, suggesting they are potentially restricted to endosymbiotic environments.

Keywords

Symbiodinium Dinoflagellate Chloroplast ribosomal 23S Hypervariable region of DomainV (cp23S-HVR) 

Supplementary material

338_2011_832_MOESM1_ESM.doc (306 kb)
Supplementary material 1 (DOC 305 kb)

References

  1. Adams LM, Cumbo VR, Takabayashi M (2009) Exposure to sediments enhances primary acquisition of Symbiodinium by asymbiotic coral larvae. Mar Ecol Prog Ser 377:149–156CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic logical alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  3. Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities. Mol Ecol 16:1127–1134PubMedCrossRefGoogle Scholar
  4. Baghdasarian G, Muscatine L (2000) Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biol Bull 199:278–286PubMedCrossRefGoogle Scholar
  5. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  6. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  7. Blasco D (1978) Observations on the diel migration of marine dinoflagellates off the Baja California coast. Mar Biol 46:41–47CrossRefGoogle Scholar
  8. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–325CrossRefGoogle Scholar
  9. Carlos AA, Baillie BK, Kawachi M, Maruyama TA (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
  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, Lewis CL, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbiosis with reef cnidarians. Curr Biol 16:R985–R988PubMedCrossRefGoogle Scholar
  12. Correa AMS, Baker AC (2009) Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:81–93CrossRefGoogle Scholar
  13. Díez B, Pedrós-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941PubMedCrossRefGoogle Scholar
  14. Edmunds PJ, Gates RD, Leggat W, Hoegh-Guldberg O, Allen-Requa L (2005) The effect of temperature on the size and population density of dinoflagellates in larvae of the reef coral Porites astreoides. Invertebr Biol 124:185–193CrossRefGoogle Scholar
  15. Fitt WK (1985) Effect of different strains of zooxanthellae Symbiodinium microadriaticum on growth and survival of their coelenterate and molluscan hosts. Proc 5th Int Coral Reef Symp 6:131–136Google Scholar
  16. Gou W, Sun J, Zhen Y, Xin Z, Yu Z, Li R (2003) Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, P.R. China. J Exp Mar Biol Ecol 296:135–144CrossRefGoogle Scholar
  17. Goulet TL, Simmons C, Goulet D (2008) Worldwide biogeography of Symbiodinium in tropical octocorals. Mar Ecol Prog Ser 355:45–58CrossRefGoogle Scholar
  18. Granados C, Camargo C, Zea S, Sánchez JA (2008) Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean. Mol Phylogenet Evol 49:554–560PubMedCrossRefGoogle Scholar
  19. Gray JS (1988) Organelle origins and ribosomal RNA. Biochem Cell Biol 66:325–348PubMedCrossRefGoogle Scholar
  20. GuoFu C, GuangCe W, ChunYun Z, BaiCheng Z (2008) Morphological and phylogenetics analysis of a Gymnodinium-like species from the Chinese Coast. Chin Sci Bull 53:561–567CrossRefGoogle Scholar
  21. 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
  22. Harris EH, Boynton JE, Gillham NW (1994) Chloroplast ribosomes and protein synthesis. Microbiol Rev 58:700–754PubMedGoogle Scholar
  23. Harrison PL, Wallace CC (1990) Coral reproduction. In: Dubinsky Z (ed) Ecosystems of the world: coral reefs. Elsevier, AmsterdamGoogle Scholar
  24. Hill R, Ralph PJ (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 352:137–144CrossRefGoogle Scholar
  25. Hill M, Allenby A, Ramsby B, Schonberg C, Hill A (2011) Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol Phylogenet Evol 59:81–88PubMedCrossRefGoogle Scholar
  26. Hirose M, Yamamoto H, Nonaka M (2008a) Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp. Coral Reefs 27:247–254CrossRefGoogle Scholar
  27. Hirose M, Reimer JD, Hidaka M, Suda S (2008b) Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar Biol 155:105–112CrossRefGoogle Scholar
  28. Jones R, Yellowlees JD (1997) Regulation and control of intracellular algae (zooxanthellae) in hard corals. Philos Trans R Soc Lond Ser B 352:457–468CrossRefGoogle Scholar
  29. Kinzie RA III, Chee GS (1979) The effect of different zooxanthellae on the growth of experimentally reinfected hosts. Biol Bull 156:315–327PubMedCrossRefGoogle Scholar
  30. Kinzie RA III, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: Experimental tests of critical assumptions. Biol Bull 200:51–58PubMedCrossRefGoogle Scholar
  31. Koike K, Yamashita H, Oh-Uchi A, Tamaki M, Hayashibara T (2007) A quantitative real-time PCR method for monitoring Symbiodinium in the water column. Galaxea 9:1–12CrossRefGoogle Scholar
  32. Krupp DA (1983) Sexual reproduction and early development of the solitary coral Fungia scutaira (Antozoa: Scleractinia). Coral Reefs 2:159–164CrossRefGoogle Scholar
  33. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  34. 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
  35. 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
  36. 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
  37. Li WKW (2002) Macroecological patterns of phytoplankton in the northwestern North Atlantic Ocean. Nature 419:154–157PubMedCrossRefGoogle Scholar
  38. Little F, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedCrossRefGoogle Scholar
  39. Littman RA, van Oppen MJH, Willis BL (2008) Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J Exp Mar Biol Ecol 364:48–53CrossRefGoogle Scholar
  40. Manning M, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861CrossRefGoogle Scholar
  41. Moreira D, López-García P (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol 10:31–38PubMedCrossRefGoogle Scholar
  42. Mouritsen LT, Richardson K (2003) Vertical microscale patchiness in nano- and microplankton distributions in a stratified estuary. J Plankton Res 25:783–797CrossRefGoogle Scholar
  43. Muscatine L, Porter JW (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  44. Nozawa Y, Harrison PL (2005) Temporal settlement patterns of larvae of the broadcast spawning reef coral Favites chinensis and the broadcast spawning and brooding reef coral Goniastrea aspera from Okinawa, Japan. Coral Reefs 24:274–282CrossRefGoogle Scholar
  45. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497PubMedCrossRefGoogle Scholar
  46. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodiniumlike endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078Google Scholar
  47. Pochon X, LaJeunesse TC, Pawloski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27CrossRefGoogle Scholar
  48. Pochon X, Montoya-Burgos 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
  49. Pochon X, Garcia-Cuetos L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867–882CrossRefGoogle Scholar
  50. Pochon X, Stat M, Takabayashi M, Chasqui L, Chauka L, Logan D, Gates R (2010) Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J Phycol 46:53–65CrossRefGoogle Scholar
  51. Porto I, Granados C, Restrepo JC, Sanchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS ONE 3:e2160PubMedCrossRefGoogle Scholar
  52. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical Pacific and the Red Sea. Mar Ecol Prog Ser 60:185–203CrossRefGoogle Scholar
  53. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742PubMedCrossRefGoogle Scholar
  54. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269PubMedCrossRefGoogle Scholar
  55. Samanata D, Mukhopadhyay D, Chowdhury S, Ghosh J, Pal S, Basu A, Bhattacharya A, Das A, Das D, DasGupta C (2008) Protein folding by Domain V of Escherichia coli 23S rRNA: Specificity of RNA-protein interactions. J Bacteriol 190:3344–3352CrossRefGoogle Scholar
  56. Santos SR, Taylor DJ, Coffroth MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. J Phycol 37:900–912CrossRefGoogle Scholar
  57. Santos SR, Taylor DJ, Kinzie RA III, 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
  58. Santos SR, Guiterrez-Rodriguez C, Coffroth MA (2003) Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in Domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences. Mar Biotechnol 5:130–140PubMedGoogle Scholar
  59. Schönberg CHL, Loh W (2005) Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis Thele, 1900. Mar Ecol Prog Ser 299:157–166CrossRefGoogle Scholar
  60. Schönberg CHL, Suwa R, Hidaka M, Loh WKW (2008) Sponge and coral zooxanthellae in heat and light: preliminary results of photochemical efficiency monitored with pulse amplitude modulated fluorometry. Mar Ecol 29:247–258CrossRefGoogle Scholar
  61. 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
  62. Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Nat Acad Sci USA 105:9256–9261PubMedCrossRefGoogle Scholar
  63. Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96CrossRefGoogle Scholar
  64. Stimson J, Kinzie R (1991) The diel pattern of release of zooxanthellae by colonies of Pocillopora damicornis maintained under control and nitrogen-enriched conditions. J Exp Mar Biol Ecol 153:63–74CrossRefGoogle Scholar
  65. Taylor FJR, Hoppenrath M, Saldarriaga JF (2008) Dinoflagellate diversity and distribution. Biodivers Conserv 17:407–418CrossRefGoogle Scholar
  66. Thornhill DJ, Lajeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems” how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340PubMedCrossRefGoogle Scholar
  67. Thornhill DJ, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS One 4:e6262PubMedCrossRefGoogle Scholar
  68. Unrein F, Izaguirre I, Massana R, Balagué V, Gasol JM (2005) Nanoplankton assemblages in maritime Antarctic lakes: characterization and molecular fingerprinting comparison. Aqua Microb Ecol 40:269–282CrossRefGoogle Scholar
  69. van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487CrossRefGoogle Scholar
  70. Venera-Ponton DE, Diaz-Pulido G, Rodriguez-Lanetty M, Hoegh-Guldberg O (2010) Presence of Symbiodinium spp. in macroalgal microhabitats from the southern Great Barrier Reef. Coral Reefs 29:1049–1060CrossRefGoogle Scholar
  71. Werner U, Blazejak A, Bird P, Eickert G, Schoon R, Abed RMM, Bissett A, de Beer D (2008) Microbial photosynthesis in coral reef sediments (Heron Reef, Australia). Estuar Coast Shelf Sci 76:876–888CrossRefGoogle Scholar
  72. Yacobovitch T, Benayahu Y, Weis VM (2004) Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria). J Exp Mar Biol Ecol 298:35–48CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • M. Takabayashi
    • 1
  • L. M. Adams
    • 1
  • X. Pochon
    • 2
  • R. D. Gates
    • 2
  1. 1.Marine Science DepartmentUniversity of Hawai‘i at HiloHiloUSA
  2. 2.Hawai‘i Institute of Marine BiologyUniversity of Hawai‘i at MānoaKāne‘oheUSA

Personalised recommendations