Skip to main content

Advertisement

Log in

Symbiodinium diversity in the soft coral Heteroxenia sp. and its nudibranch predator Phyllodesmium lizardensis

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

Abstract

We examined the diversity of the photosynthetic dinoflagellate, Symbiodinium, over a 2-year period in two invertebrates from Australia’s Northern Great Barrier Reef: the nudibranch Phyllodesmium lizardensis and an octocoral of the genus Heteroxenia. In years one and two, we used denaturing gradient gel electrophoresis with internal transcribed spacer 2 (ITS2) region amplicons and identified two nearly identical genotypes of clade C (C64 and a variant) in all samples of each species. We examined the secondary structure of both sequences and found that each had predicted ∆G values within the range of stable free energy values for Symbiodinium ITS2 sequences. In year two, we also used real-time quantitative polymerase chain reaction assays (qPCR) with clade-specific internal transcribed spacer 1 primers to determine whether there were cryptic clades (A, B, and/or D) associated with either host in addition to clade C. qPCR revealed that clades B, C, and D were present in all animals of both species and that all but two nudibranch samples also harbored clade A. These findings suggest that there may be more flexibility in this host/symbiont interaction than has previously been assumed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol Phylogenet Evol 29:435–455

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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 335:237–242

    Article  Google Scholar 

  • Barneah O, Weis VM, Perez S, Benayahu Y (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition maters. Mar Ecol Prog Ser 275:89–95

    Article  CAS  Google Scholar 

  • Barneah O, Brickner I, Hooge M, Weis VM, LaJeunesse TC, Benayahu Y (2007) Three party symbiosis: acoelomorph worms, corals and unicellular algal symbionts in Eilat (Red Sea). Mar Biol 151:1215–1223

    Article  Google Scholar 

  • Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc Lond 273:2305–2312

    Article  Google Scholar 

  • Burghardt I, Schrödl M, Wägele H (2008a) Three new solar-powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidioidea) from the tropical Indo-Pacific, with analysis of their photosynthetic activity and notes on biology. J Molluscan Stud 74:277–292

    Article  Google Scholar 

  • Burghardt I, Stemmer K, Wäegele H (2008b) Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analyses of long-term retention. Org Divers Evol 8:66–76

    Article  Google Scholar 

  • Bustin SA (2004) A-Z of Quantitative PCR, vol 5, 1st edn. International University Line, San Diego

    Google Scholar 

  • Chen CA, Lam KK, Nakano Y, Tsai WS (2003) Stable association of a stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature tolerant coral, Oulastrea crispata, in subtropical nonreefal coral communities. Zool Stud 42:540–550

    Google Scholar 

  • Chen CA, Wang J, Fang L, Yang Y (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Coleman AW, Suarez AS, Goff LJ (1994) Molecular delineation of species and syngens in volvocacean green algae (Chlorophyta). J Phycol 30:80–90

    Article  CAS  Google Scholar 

  • D’Croz LD, Maté JL (2004) Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23:473–483

    Article  Google Scholar 

  • Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) ‘Touchdown’ PCR to prevent spurious priming during gene amplification. Nucleic Acids Res 19:4008

    Article  PubMed  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl M, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  CAS  Google Scholar 

  • Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2011) GeoSymbio: a hybrid, cloud‐based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses. Mol Ecol Res 12:369–373

    Article  Google Scholar 

  • Giovannoni SJ, DeLong EF, Schmidt TM, Pace NR (1990) Tangential flow filtration and preliminary phylogenetic analysis of marine picoplankton. Appl Environ Microbiol 56:2572–2575

    PubMed  CAS  Google Scholar 

  • Goulet TL (2006) Most corals may not change their symbionts. Mar Ecol Prog Ser 321:1–7

    Article  Google Scholar 

  • Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498

    Article  CAS  Google Scholar 

  • Goulet TL, LaJeunesse TC, Fabricius KE (2008) Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Mar Biol 154:795–804

    Article  Google Scholar 

  • Hallock P (2001) Coral reefs, carbonate sediments, nutrients and global change. In: Stanley GD Jr (ed) The history and sedimentology of ancient reef systems. Springer, New York, pp 387–427

    Chapter  Google Scholar 

  • 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 

  • Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the World’s marine ecosystems. Science 328:1523–1528

    Article  PubMed  CAS  Google Scholar 

  • Howells EJ, van Oppen MJH, Willis BL (2009) High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs 28:215–225

    Article  Google Scholar 

  • Hunter RL, LaJeunesse TC, Santos SR (2007) Structure and evolution of the rDNA internal transcribed spacer (ITS) region 2 in the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 43:120–128

    Article  CAS  Google Scholar 

  • Iglesias-Prieto R, Matta JL, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305

    Article  PubMed  CAS  Google Scholar 

  • Jackson CR, Roden EE, Churchill PF (2000) Denaturing gradient gel electrophoresis can fail to separate 16S rDNA fragments with multiple base differences. Mol Biol Today 1:49–51

    CAS  Google Scholar 

  • Kempf SC (1984) Symbiosis between the zooxanthella Symbiodinium (=Gymnodinium) microadriaticum (Freudenthal) and four species of nudibranchs. Biol Bull 166:110–126

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581

    Article  PubMed  CAS  Google Scholar 

  • LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134

    Article  PubMed  CAS  Google Scholar 

  • LaJeunesse TC, Loh WKW, 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 48:2046–2054

    Article  Google Scholar 

  • LaJeunesse TC, Bhagooli R, Hidaka M, Done T, deVantier L, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely-related Symbiodinium spp. differ in relative dominance within coral reef host communities across environmental, latitudinal, and biogeographic gradients. Mar Ecol Prog Ser 284:147–161

    Article  Google Scholar 

  • LaJeunesse TC, Pettay T, 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 

  • Lewis CL, Coffroth MA (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304:1490–1492

    Article  PubMed  CAS  Google Scholar 

  • Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    Article  PubMed  CAS  Google Scholar 

  • Loh WKW, Cowlishaw M, Wilson NG (2006) Diversity of Symbiodinium dinoflagellate symbionts from the Indo-Pacific sea slug Pteraeolidia ianthina (Gastropoda: Mollusca). Mar Ecol Prog Ser 320:177–184

    Article  CAS  Google Scholar 

  • Loram JE, Trapido-Rosenthal HG, Douglas AE (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol Ecol 16:4849–4857

    Article  PubMed  CAS  Google Scholar 

  • Magalon H, Flot JF, Baudry E (2007) Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551–558

    Article  Google Scholar 

  • 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 26:449–457

    Article  Google Scholar 

  • Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    Article  CAS  Google Scholar 

  • Norton JH, Shepherd MA, Long HM, Fitt WK (1992) The zooxanthellal tubular system in the giant clam. Biol Bull 183:503–506

    Article  Google Scholar 

  • Peculis BA, Greer CL (1998) The structure of the ITS2-proximal stem is required for pre-rRNA processing in yeast. RNA 4:1610–1622

    Article  PubMed  CAS  Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    Article  PubMed  CAS  Google Scholar 

  • Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27

    Article  Google Scholar 

  • Robison J, Warner M (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579

    Article  CAS  Google Scholar 

  • Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiatrea versipora. Mar Biol 138:1176–1181

    Google Scholar 

  • Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Mar Biol 153:225–234

    Google Scholar 

  • Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal algal symbiosis. Science 251:1348–1351

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 23:97–111

    Article  PubMed  CAS  Google Scholar 

  • Savage AM, Trapido-Rosenthal H, Douglas AE (2002) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Mar Ecol Prog Ser 244:27–37

    Article  Google Scholar 

  • Sawyer SJ, Muscatine L (2001) Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 204:3443–3456

    PubMed  CAS  Google Scholar 

  • Schwarz JA, Weis VM (2003) Immunolocalization of host sym32 and an undescribed protein, p45/48, in the sea anemone-dinoflagellate association Anthopleura elegantissima- Symbiodinium muscatinei. Biol Bull 205:339–350

    Article  PubMed  CAS  Google Scholar 

  • Stat M, Carter DA, 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 8:23–43

    Article  Google Scholar 

  • Stat M, Bird CE, Pochon X, Chesqui L, Chauka LJ, Concepcion GT, Logan D, Takabayashi M, Toonen RJ, Gates R (2011) Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS ONE 6:e15854

    Article  PubMed  CAS  Google Scholar 

  • Steindler L, Beer S, Ilan M (2002) Photosymbiosis in intertidal and subtidal tropical sponges. Symbiosis 33:263–273

    Google Scholar 

  • Strychar KB, Coates M, Sammarco PW, Piva TJ (2004) Bleaching as a pathogenic response in scleractinian corals, evidenced by high concentrations of apoptotic and necrotic zooxanthellae. J Exp Mar Biol Ecol 304:99–121

    Article  Google Scholar 

  • Strychar KB, Coates M, Sammarco PW, Piva TJ, Scott PT (2005) Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp. and Xenia sp. J Exp Mar Biol Ecol 320:159–177

    Article  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Yadav SW, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535

    Article  PubMed  CAS  Google Scholar 

  • Thornhill D, LaJeunesse TC, Santos CR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340

    Article  PubMed  CAS  Google Scholar 

  • 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 12:3477–3484

    Article  PubMed  CAS  Google Scholar 

  • Ulstrup KE, van Oppen MJH, Kühl M, Ralph PJ (2007) Inter-polyp genetic and physiological characterisation of Symbiodinium in an Acropora valida colony. Mar Biol 153:225–234

    Article  Google Scholar 

  • van Oppen MJH, Mieog JC, Sanchez CA, Fabricus KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417

    Article  PubMed  Google Scholar 

  • Varani G, McClain W (2002) The G.U wobble base pair: A fundamental building block of RNA structure crucial to RNA function in diverse biological systems. EMBO Rep 1:18–23

    Article  Google Scholar 

  • Venn AA, Lorem JE, Trapido-Rosenthal HG, Joyce DA, Douglas AE (2008) Importance of time and place: patterns in abundance of Symbiodinium clades A and B in the tropical sea anemone Condylactis gigantea. Biol Bull 215:243–252

    Article  PubMed  CAS  Google Scholar 

  • Waegele H, Vonnemann V, Waegele JW (2003) Towards a phylogeny of the Opisthobranchia. In: Lydeard C, Lindberg D (eds) Molecular systematics and phylogeography of mollusks. Smithsonian Institution Press, Washington, DC, pp 185–228

    Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Google Scholar 

Download references

Acknowledgments

We appreciate the BURR Culture Collection and the Lizard Island Research Station staff for their generous help. We would also like to recognize the Great Barrier Reef Marine Park Authority for facilitating permit acquisition. Special thanks to Erin Crossey and Carmela Carrasco for technical support and Dr. David Hanson for his assistance in maintaining the algal cultures. This work was funded in part by a grant from the National Science Foundation (ID0436605), a National Institutes for Health Post-Baccalaureate Research Education grant to KLL (R25GM075149), a UNM Research Allocations grant, and an anonymous donation to the University of New Mexico’s Department of Biology. Technical support for sequencing and qPCR was provided by the University of New Mexico’s Molecular Biology Facility, which is supported by National Institutes of Health grant 1P20RR18754 from the Institute Development Award Program of the National Center for Research Resources. We also thank three anonymous reviewers for their comments and constructive criticism, which have greatly improved this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to U. L. Shepherd.

Additional information

Communicated by Biology Editor Dr. Ruth Gates

S. K. FitzPatrick and K. L. Liberatore contributed equally to the research performed here.

Rights and permissions

Reprints and permissions

About this article

Cite this article

FitzPatrick, S.K., Liberatore, K.L., Garcia, J.R. et al. Symbiodinium diversity in the soft coral Heteroxenia sp. and its nudibranch predator Phyllodesmium lizardensis . Coral Reefs 31, 895–905 (2012). https://doi.org/10.1007/s00338-012-0913-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-012-0913-0

Keywords

Navigation