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Biology of Symbiotic Dinoflagellates (Symbiodinium) in Corals

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Marine Protists

Abstract

The chapter summarizes the diversity and ecology of zooxanthellae, especially focusing on the dinoflagellate genus Symbiodinium. Symbiodinium spp. are known to engage in mutual symbioses with a wide variety of marine invertebrates (e.g., corals) and protists, in both tropical and temperate waters. Because of an increasing awareness of “coral bleaching” (death of corals due to loss of symbiotic algae), there have been many investigations into Symbiodinium and coral interactions. In this chapter, the taxonomy and general ecology of Symbiodinium are initially described, followed by recent genetic classification systems, which have contributed to a clearer understanding of Symbiodinium diversity and its host specificity. Finally, mechanisms of both symbiotic initiation and breakdown in association with corals are highlighted, to predict the future of coral reef ecosystems in the changing ocean environments.

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References

  • Abrego D, van Oppen MJH, Willis BL (2009a) Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol 18:3518–3531

    Article  PubMed  Google Scholar 

  • Abrego D, van Oppen MJH, Willis BL (2009b) Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol Ecol 18:3532–3543

    Article  PubMed  Google Scholar 

  • Adams LM, Cumbo VR, Takabayashi M (2009) Exposure to sediments enhances primary acquisition of Symbiodinium by asymbiotic coral larvae. Mar Ecol Prog Ser 377:149–156

    Article  Google Scholar 

  • 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 

  • Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741

    Article  CAS  PubMed  Google Scholar 

  • Banaszak AT, Trench RK (1995) Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. I. Response of the algal symbionts in culture and in hospite. J Exp Mar Biol Ecol 194:213–232

    Article  Google Scholar 

  • Barnes DJ, Chalker BE (1990) Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky Z (ed) Coral reefs ecosystems of the world, vol 25. Elsevier, Amsterdam, pp 109–131

    Google Scholar 

  • Bay LK, Howells EJ, van Oppen MJH (2009) Isolation, characterization and cross amplification of thirteen microsatellite loci for coral endo-symbiotic dinoflagellates (Symbiodinium clade C). Conserv Genet Resour 1:199–203

    Article  Google Scholar 

  • Bhagooli R, Hidaka M (2004) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar Biol 145:329–337

    Article  CAS  Google Scholar 

  • Blank RJ, Huss VAR (1989) DNA divergency and speciation in Symbiodinium (Dinophyceae). Plant Syst Evol 163:153–163

    Article  Google Scholar 

  • Blank RJ, Trench RK (1986) Nomenclature of endosymbiotic dinoflagellates. Taxon 35:286–294

    Article  Google Scholar 

  • Brandt K (1881) Über das Zusammenleben von Thieren und Algen Verh Physiologischen Ges. Berlin. 1881–1882: 22–26

    Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • Brown BE, Le Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar Biol 122:655–663

    Article  Google Scholar 

  • Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326

    Article  Google Scholar 

  • 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 35:1054–1062

    Article  CAS  Google Scholar 

  • Carlos AA, Baillie BK, Maruyama T (2000) Diversity of dinoflagellate symbionts (zooxanthellae) in a host individual. Mar Ecol Prog Ser 195:93–100

    Article  Google Scholar 

  • Clode PL, Saunders M, Maker G, Ludwig M, Atkins C (2009) Uric acid deposits in symbiotic marine algae. Plant Cell Environ 32:170–177

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16:R985–R987

    Article  CAS  PubMed  Google Scholar 

  • Correa AMS, McDonald MD, Baker AC (2009) Development of lade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol 156:2403–2411

    Article  CAS  Google Scholar 

  • Crossland CJ (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–42

    Article  CAS  Google Scholar 

  • Cumbo VR, Baird AH, van Oppen MJH (2013) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120

    Article  Google Scholar 

  • Egaña AC, DiSalvo LH (1982) Mass expulsion of zooxanthellae by Easter Island corals. Pac Sci 36:61–63

    Google Scholar 

  • Ferrier-Pagès C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274

    Article  Google Scholar 

  • Finney JC, Pettay T, Sampayo EM, Warner ME, Oxenford H, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism and speciation of coral endosymbionts. Microb Ecol 60:250–263

    Article  PubMed  Google Scholar 

  • 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 

  • Frade PR, Engelbert N, Faria J, Visser PM, Bak RPM (2008) Distribution and photobiology of Symbiodinium types in divergent light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27:913–925

    Article  Google Scholar 

  • Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses. Mol Ecol Resour 12:369–373

    Article  PubMed  Google Scholar 

  • Freudenthal HD (1962) Symbiodinium gen nov and Symbiodinium microadriaticum sp nov, a zooxanthella—taxonomy, life cycle, and morphology. J Protozool 9:45–52

    Article  Google Scholar 

  • Fujise L, Yamashita H, Suzuki G, Koike K (2014) Expulsion of zooxanthellae (Symbiodinium) from several species of scleractinian corals: comparison under non-stress conditions and thermal stress conditions. Galaxea 15:1–8

    Google Scholar 

  • Fujise L, Yamashita H, Suzuki G, Sasaki K, Liao LM, Koike K (2015) Moderate thermal stress causes active and immediate expulsion of photosynthetically damaged zooxanthellae (Symbiodinium) from corals. PLoS One 9, e114321

    Article  CAS  Google Scholar 

  • Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332

    Article  Google Scholar 

  • Glynn PW, Maté JL, Baker AC, Calderón MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

  • Gómez-Cabrera MC, Ortiz JC, Loh WKW, Ward S, Hoegh-Guldberg O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27:219–226

    Article  Google Scholar 

  • Goreau TF (1964) Mass expulsion of zooxanthellae from Jamaican reef communities after hurricane Flora. Science 145:383–386

    Article  CAS  PubMed  Google Scholar 

  • Goreau TJ, Hayes RL (1994) Coral bleaching and ocean ‘Hot Spots’. Ambio 23:176–180

    Google Scholar 

  • Hansen G, Daugbjerg N (2009) Symbiodinium natans sp. nov.: a “free-living” dinoflagellate from Tenerife (Northeast-Atlantic Ocean). J Phycol 45:251–263

    Article  Google Scholar 

  • Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195

    Article  Google Scholar 

  • Hikosaka-Katayama T, Koike K, Yamashita H, Hikosaka A, Koike K (2012) Mechanisms of maternal inheritance of dinoflagellate symbionts in the Acoelomorph worm Waminoa litus. Zool Sci 29:559–567

    Article  PubMed  Google Scholar 

  • Hill R, Ralph PJ (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 352:137–144

    Article  Google Scholar 

  • Hill M, Wilcox T (1998) Unusual mode of symbiont repopulation after bleaching in Anthosigmella varians: acquisition of different zooxanthellae strains. Symbiosis 25:279–289

    Google Scholar 

  • Hirose M, Hidaka M (2006) Early development of zooxanthella-containing eggs of the corals Porites cylindrica and Montipora digitata: the endodermal localization of zooxanthellae. Zool Sci 23:873–881

    Article  PubMed  Google Scholar 

  • Hirose M, Yamamoto H, Nonaka M (2008) Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp. Coral Reefs 27:247–254

    Article  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, Smith GJ (1989) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol 129:279–303

    Article  Google Scholar 

  • Hunter CL, Morden CW, Smith CM (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. In: Proceedings of the 8th international coral reef symposium, vol 2, pp 1599–1602

    Google Scholar 

  • Ishikura M, Adachi K, Maruyama T (1999) Zooxanthellae release glucose in the tissue of a giant clam, Tridacna crocea. Mar Biol 133:665–673

    Article  CAS  Google Scholar 

  • Jaap WC (1979) Observations on zooxanthellae expulsion at Middle Sambo Reef, Florida Keys. Bull Mar Sci 29:412–422

    Google Scholar 

  • Jeong HJ, Yoo YD, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin WG, Nam SW, Yih WH, Lee K (2012) Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Natl Acad Sci U S A 109:12604–12609

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, Kim HS, Yih W, Yamashita H, LaJeunesse TC (2014) Genetics and morphology characterize the Dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. J Eukaryot Microbiol 61:75–94

    Article  CAS  PubMed  Google Scholar 

  • Jimbo M, Yanohara 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 Part B 125:227–236

    Article  CAS  Google Scholar 

  • Jimbo M, Yamashita H, Koike K, Sakai R, Kamiya H (2010) Effects of lectin in the scleractinian coral Ctenactis echinata on symbiotic zooxanthellae. Fish Sci 76:355–363

    Article  CAS  Google Scholar 

  • Jimbo M, Suda Y, Koike K, Nakamura-Tsuruta S, Kominami J, Kamei M, Hirabayashi J, Sakai R, Kamiya H (2013) Possible involvement of glycolipids in lectin- mediated cellular transformation of symbiotic microalgae in corals. J Exp Mar Biol Ecol 439:129–135

    Article  CAS  Google Scholar 

  • Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B 275:1359–1365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kawaguti S (1944) On the physiology of reef corals VII. Zooxanthella of the reef coral is Gymnodinium sp., Dinoflagellata; its culture in vitro. Palao Trop Biol Stn Stud 2:675–679

    Google Scholar 

  • Kinzie RA, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull 200:51–58

    Article  PubMed  Google Scholar 

  • Klumpp DW, Lucas JS (1994) Nutritional ecology of the giant clams Tridacna teboroa and T. derasa from Tonga: influence of light on filter-feeding and photosynthesis. Mar Ecol Prog Ser 107:147–156

    Article  Google Scholar 

  • Kobluk DR, Lysenko MA (1994) “Ring” bleaching in southern Caribbean Agaricia agaricites during rapid water cooling. Bull Mar Sci 54:142–150

    Google Scholar 

  • Koike K, Jimbo M, Sakai R, Kaeriyama M, Muramoto K, Ogata T, Maruyama T, Kamiya H (2004) Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biol Bull 207:80–86

    Article  CAS  PubMed  Google Scholar 

  • 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 9:1–12

    Article  Google Scholar 

  • Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and coral bleaching. Nature 380:396

    Article  CAS  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, Trench RK (2000) The biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal anemone, Anthopleura elegantissima (Brandt). Biol Bull 199:126–134

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura D, Hoegh-Guldberg O, Fitt WK (2010) 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 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 364:48–53

    Article  Google Scholar 

  • Lobban CS, Schefter M, Simpson AGB, Pochon X, Pawlowski J, Foissner W (2002) Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Mar Biol 140:411–423

    Article  Google Scholar 

  • Loeblich AR III, Sherley JL (1979) Observations on the theca of the motile phase of free-living and symbiotic isolates of Zooxanthella microadriatica (Freudenthal) comb. nov. J Mar Biol Assoc UK 59:195–205

    Article  Google Scholar 

  • Maruyama T, Heslinga GA (1997) Fecal discharge of zooxanthellae in the giant clam Tridacna derasa, with reference to their in situ growth rate. Mar Biol 127:473–477

    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 (1967) Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science 156:516–519

    Article  CAS  PubMed  Google Scholar 

  • Nakajima R, Yoshida T, Azman BAR, Zaleha K, Othman BHR, Toda T (2009) In situ release of coral mucus by Acropora and its influence on the heterotrophic bacteria. Aquat Ecol 43:815–823

    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 

  • Pawlowski J, Holzmann M, Fahrni JF, Pochon X, Lee JJ (2001) Molecular identification of algal endosymbionts in large miliolid foraminifera: 2. Dinoflagellates. J Eukaryot Microbiol 48:368–373

    Article  CAS  PubMed  Google Scholar 

  • Pinzón JH, Devlin-Durante MK, Weber XM, Baums IB, LaJeunesse TC (2011) Microsatellite loci for Symbiodinium A3 (S. fitti) a common algal symbiont among Caribbean Acropora (stony corals) and Indo-Pacific giant clams (Tridacna). Conserv Genet Resour 3:45–47

    Article  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  CAS  PubMed  Google Scholar 

  • 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 Hawaiian reef environment. J Phycol 46:53–65

    Article  CAS  Google Scholar 

  • Podestá GP, Glynn PW (1997) Sea surface temperature variability in Panamá and Galápagos: extreme temperatures causing coral bleaching. J Geophys Res 102:15749–15759

    Article  Google Scholar 

  • Reimer JD, Shah MMR, Sinniger F, Yanagi K, Suda S (2010) Preliminary analyses of cultured Symbiodinium isolated from sand in the oceanic Ogasawara Islands, Japan. Mar Biodivers 40:237–247

    Article  Google Scholar 

  • Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417

    Article  Google Scholar 

  • Rowan R (2004) Thermal adaptations in reef coral symbionts. Nature 430:742

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rowan R, Powers DA (1991b) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Rowan R, Powers DA (1992) Ribosomal-RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc Natl Acad Sci U S A 89:3639–3643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269

    Article  CAS  PubMed  Google Scholar 

  • Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Gulberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Santos SR, Coffroth MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biol Bull 204:10–20

    Article  CAS  PubMed  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002a) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111

    Article  CAS  PubMed  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RA III, Sakai K, Coffroth MA (2002b) Evolution of length variation and heteroplasmy in the chloroplast rDNA of symbiotic dinoflagellates (Symbiodinium, Dinophyta) and a novel insertion in the universal core region of the large subunit rDNA. Phycologia 41:311–318

    Article  Google Scholar 

  • 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 13:459–469

    Article  CAS  PubMed  Google Scholar 

  • Schoenberg DA, Trench RK (1980a) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of S. microadriaticum. Proc R Soc Lond B 207:405–427

    Article  CAS  Google Scholar 

  • Schoenberg DA, Trench RK (1980b) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. II. Morphological variation in S. microadriaticum. Proc R Soc Lond B 207:429–444

    Article  Google Scholar 

  • Schoenberg DA, Trench RK (1980c) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc R Soc Lond B 207:445–460

    Article  Google Scholar 

  • Silverstein RN, Correa AMS, Baker AC (2012) Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc R Soc B 279:2609–2618

    Article  PubMed Central  PubMed  Google Scholar 

  • Steele RD (1975) Stages in the life history of a symbiotic zooxanthellae in pellets extruded by its host Aiptasia tagetes (Duch. and Mich.) (Coelenterata, Anthozoa). Biol Bull 149:590–600

    Article  Google Scholar 

  • Steen RG, Muscatine L (1987) Low temperature evokes rapid exocytosis of symbiotic algae by a sea anemone. Biol Bull 172:246–263

    Article  Google Scholar 

  • Stern RF, Horak A, Andrew RL, Coffroth MA, Andersen RA, Kupper FC, Jameson I, Hoppenrath M, Veron B, Kasai F, Brand J, James ER, Keeling PJ (2010) Environmental barcoding reveals massive dinoflagellate diversity in marine environments. PLoS One 5:e13991

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164

    Article  CAS  Google Scholar 

  • Takabayashi M, Adams LM, Pochon X, Gates RD (2011) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai’i and Florida. Coral Reefs 31:157–167

    Article  Google Scholar 

  • Takishita K, Ishikura M, Koike K, Maruyama T (2003) Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium. Phycologia 42:285–291

    Article  Google Scholar 

  • Tanaka Y, Miyajima T, Koike I, Hayashibara T, Ogawa H (2006) Translocation and conservation of organic nitrogen within the coral–zooxanthella symbiotic system of Acropora pulchra, as demonstrated by dual isotope-labeling techniques. J Exp Mar Biol Ecol 336:110–119

    Article  CAS  Google Scholar 

  • Tanaka Y, Miyajima T, Umezawa Y, Hayashibara T, Ogawa H, Koike I (2009) Net release of dissolved organic matter by the scleractinian coral Acropora pulchra. J Exp Mar Biol Ecol 377:101–106

    Article  CAS  Google Scholar 

  • Taylor DL (1968) In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate. J Mar Biol Assoc UK 48:349–366

    Article  Google Scholar 

  • Taylor DL (1971) Ultrastructure of the “zooxanthella” Endodinium chattonii in situ. J Mar Biol Assoc UK 51:227–234

    Article  Google Scholar 

  • Taylor DL (1974) Symbiotic marine algae; taxonomy and biological fitness. In: Vernberg WB (ed) Symbiosis in the Sea. University of South Carolina Press, Columbia, pp 245–262

    Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, 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 U S A 101:13531–13535

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thornhill DJ, Lewis A, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367

    Article  CAS  PubMed  Google Scholar 

  • Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, Yamazato K (1996) Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol Prog Ser 139:167–178

    Article  Google Scholar 

  • Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease associated bleaching. Biol Bull 201:360–373

    Article  CAS  PubMed  Google Scholar 

  • Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pagès C (2012) Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215:1384–1393

    Article  CAS  PubMed  Google Scholar 

  • Trench RK (1987) Dinoflagellates in non-parasitic symbioses. In: Taylor FJR (ed) The biology of the dinoflagellates. Blackwell, Oxford, pp 530–570

    Google Scholar 

  • Trench RK (1993) Microalgal-invertebrate symbiosis: a review. Endocytobiosis Cell Res 9:135–175

    Google Scholar 

  • Trench RK (1997) Diversity of symbiotic dinoflagellates and the evolution of microalgal- invertebrate symbioses. In: Proceedings of the 8th international coral reef symposium, vol 2, pp 1275–1286

    Google Scholar 

  • Trench RK (2000) Validation of some currently used invalid names of dinoflagellates. J Phycol 36:972

    Article  Google Scholar 

  • Trench RK, Blank RJ (1987) Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov.: Gymnodinioid dinoflagellate symbionts of marine invertebrates. J Phycol 23:469–481

    Article  Google Scholar 

  • Trench RK, Thinh LV (1995) Gymnodinium linucheae sp. nov.: the dinoflagellate symbiont of the jellyfish Linuche unguiculata. Eur J Phycol 30:149–154

    Article  Google Scholar 

  • Trench RK, Wethey DS, Porter JW (1981) Observation on the symbiosis with zooxanthellae among the Tridacnidae (Mollusca, Bivalvia). Biol Bull 161:180–198

    Article  Google Scholar 

  • van Oppen MJH, Palstra FP, Piquet A-T, 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 268:1759–1767

    Article  Google Scholar 

  • Vidal-Dupiol J, Adjeroud M, Roger E, Foure L, Duval D, Mone Y, Ferrier-Pages C, Tambutte E, Tambutte S, Zoccola D, Allemand D, Mitta G (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physiol 9:14

    Article  PubMed Central  PubMed  Google Scholar 

  • Wham DC, Carmichael M, LaJeunesse TC (2013) Microsatellite loci for Symbiodinium goreaui and other Clade C Symbiodinium. Conserv Genet Resour 6:127–129

    Article  Google Scholar 

  • Wilcox TP (1998) Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny. Mol Phylogenet Evol 10:436–448

    Article  CAS  PubMed  Google Scholar 

  • Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yamashita H, Koike K (2013) Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61:68–80

    Article  CAS  Google Scholar 

  • Yamashita H, Kobiyama A, Koike K (2009) Do uric acid deposits in zooxanthellae function as eye-spots? PLoS One 4:e63003

    Article  CAS  Google Scholar 

  • Yamashita H, Suzuki G, Hayashibara T, Koike K (2011) Do corals select zooxanthellae by alternative discharge? Mar Biol 158:87–100

    Article  Google Scholar 

  • 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 

  • 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 Central  PubMed  CAS  Google Scholar 

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Yamashita, H., Koike, K. (2015). Biology of Symbiotic Dinoflagellates (Symbiodinium) in Corals. In: Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N., Not, F. (eds) Marine Protists. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55130-0_17

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