Skip to main content

Animal–Symbiodinium Symbioses: Foundations of Coral Reef Ecosystems

  • Chapter
  • First Online:
The Mechanistic Benefits of Microbial Symbionts

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 2))

Abstract

A variety of animal taxa have benefited from symbioses with photoautotrophic symbionts that provide fixed carbon in exchange for nutrients and high-light habitats. Corals are one such animal lineage, harboring dinoflagellates in the genus Symbiodinium. This genus has remarkably high genetic diversity that translates into morphological, cellular, physiological, and even host infectivity differences. Many corals acquire their symbionts as larvae or recruits upon settlement on the reef, likely from local populations of Symbiodinium present in the sediment. Onset of symbiosis is initiated by host–symbiont recognition and proceeds through a winnowing process where only suitable, healthy Symbiodinium are retained within a host-derived symbiosome membrane. High stress, as is predicted by future climate models, can lead to symbiosis dysfunction and loss of the symbiont from host tissues with negative consequences to the host. Some corals have the ability to exchange their symbiotic partners for those that may be more thermotolerant, but the extent to which coral–dinoflagellate symbioses can acclimatize and adapt to rapid climate change remains to be determined.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrego D, Willis BL, van Oppen MJH (2012) Impact of light and temperature on the uptake of algal symbionts by coral juveniles. PLoS One 7, e50311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Adl SM, Simpson AGB, Lane CE et al (2012) The revised classification of Eukaryotes. J Euk Microbiol 59:429–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Andras JP, Kirk NL, Harvell CD (2011) Range-wide population genetic structure of Symbiodinium associated with the Caribbean Sea fan coral, Gorgonia ventalina. Mol Ecol 20:2525–2542

    Article  PubMed  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G et al (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachvaroff TR, Place AR (2008) From start to stop: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 3, e2929

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bachvaroff TR, Gornik SG, Concepcion GT et al (2014) Dinoflagellate phylogeny revisited: using ribosomal proteins to resolve deep branching dinoflagellate clades. Mol Phylogenet Evol 70:314–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baird AH, Bhagooli R, Nonaka M, et al (2008) Environmental controls on the establishment and development of algal symbiosis in corals. Proceedings of the 11th international coral reef symposium 1:108–112

    Google Scholar 

  • Baird AH, Bhagooli R, Ralph PJ et al (2009a) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20

    Article  PubMed  Google Scholar 

  • Baird AH, Guest JR, Willis BL (2009b) 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) Ecosystems: reef corals bleach to survive change. Nature 411:765

    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 et al (2004) Corals’ adaptive response to climate change. Nature 430:741

    Article  CAS  PubMed  Google Scholar 

  • Banaszak AT, LaJeunesse TC, Trench RK (2000) The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J Exp Mar Biol Ecol 249:219–233

    Article  CAS  Google Scholar 

  • Barbrook AC, Visram S, Douglas AE et al (2006) Molecular diversity of dinoflagellate symbionts of cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171

    Article  CAS  PubMed  Google Scholar 

  • Barbrook AC, Voolstra CR, Howe CJ (2014) The chloroplast genome of a Symbiodinium sp. clade C3 isolate. Protist 165:1–13

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Barshis DJ, Stillman JH, Gates RD et al (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol Ecol 19:1705–1720

    Article  CAS  PubMed  Google Scholar 

  • Bay LK, Cumbo VR, Abrego D et al (2011) Infection dynamics vary between Symbiodinium types and cell surface treatments during establishment of endosymbiosis with coral larvae. Diversity 3:356–374

    Article  CAS  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 B 273:2305–2312

    Article  Google Scholar 

  • Blank RJ, Trench RK (1985) Speciation and symbiotic dinoflagellates. Science 229:656–658

    Article  CAS  PubMed  Google Scholar 

  • Boldt L, Yellowlees D, Leggat W (2012) Hyperdiversity of genes encoding integral light-harvesting proteins in the dinoflagellate Symbiodinium sp. PLoS One 7, e47456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brading P, Warner ME, Davey P et al (2011) Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol Oceanogr 56:927

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biol Lett 4:366–369

    Article  PubMed  PubMed Central  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM et al (1997) Parasitology meets ecology on its own terms: Margulis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Byler KA, Carmi-Veal M, Fine M et al (2013) Multiple symbiont acquistion strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS One 8:e59596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantin NE, van Oppen MJH, Willis BL et al (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414

    Article  Google Scholar 

  • Carlos AA, Baillie BK, Kawachi M et al (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 35:1051–1062

    Article  Google Scholar 

  • Castro-Sanguino C, Sánchez JA (2012) Dispersal of Symbiodinium by the stoplight parrotfish Sparisoma viride. Biol Lett 8:282–286

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavalier-Smith T (1991) Cell diversification in heterotrophic flagellates. In: Patterson DJ, Larson J (eds) The biology of free-living heterotrophic flagellates. Clarendon, Oxford, pp 113–131

    Google Scholar 

  • Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290

    Article  Google Scholar 

  • Chan YH, Kwok ACM, Tsang JSH et al (2006) Alveolata histone-like proteins have different evolutionary origins. J Evol Biol 19:1717–1721

    Article  CAS  PubMed  Google Scholar 

  • Chen M-C, Cheng Y-M, Sung P-J et al (2003) Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem Biophys Res Commun 308:586–595

    Article  CAS  PubMed  Google Scholar 

  • Chen M-C, Cheng Y-M, Hong M-C et al (2004) Molecular cloning of Rab5 (ApRab5) in Aiptasia pulchella and its retention in phagosomes harboring live zooxanthellae. Biochem Biophys Res Commun 324:1024–1033

    Article  CAS  PubMed  Google Scholar 

  • Chi J, Parrow MW, Dunthorn M (2014) Cryptic sex in Symbiodinium (Alveolata, Dinoflagellata) is supported by an inventory of meiotic genes. J Euk Microbiol 61:322–327

    Article  PubMed  Google Scholar 

  • Chow MH, Yan KTH, Bennett MJ et al (2010) Birefringence and DNA condensation of liquid crystalline chromosomes. Euk Cell 9:1577–1587

    Article  CAS  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 et al (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16:R985

    Article  CAS  PubMed  Google Scholar 

  • Coffroth MA, Poland DM, Petrou EL et al (2010) Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS One 5, e13258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Colley NJ, Trench RK (1983) Selectivity in phagocytosis and persistence of symbiotic algae by the scyphistoma stage of the jellyfish Cassiopeia xamachana. Proc R Soc Lond B 219:61–82

    Article  CAS  PubMed  Google Scholar 

  • Correa AMS, Baker AC (2011) Disaster taxa in microbially mediated metazoans: how endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals. Glob Change Biol 17:68–75

    Article  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 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Detournay O, Weis VM (2011) Role of the sphingosine rheostat in the regulation of cnidarian-dinoflagellate symbioses. Biol Bull 221:261–269

    CAS  PubMed  Google Scholar 

  • Detournay O, Schnitzler CE, Poole A et al (2012) Regulation of cnidarian–dinoflagellate mutualisms: evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont. Dev Comp Immunol 38:525–537

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Almeyda E, Thomé PE, El Hafidi M et al (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30:217–225

    Article  Google Scholar 

  • Douglas AE (1994) Symbiotic interactions. Oxford Science, Oxford

    Google Scholar 

  • Douglas AE (2010) The symbiotic habit. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Dunn SR, Weis VM (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ Microbiol 11:268–276

    Article  PubMed  Google Scholar 

  • Edmunds PJ, Gates RD (2008) Acclimatization in tropical reef corals. Mar Ecol Prog Ser 361:307–310

    Article  Google Scholar 

  • Edmunds PJ, Carpenter RC, Comeau S (2013) Understanding the threats of ocean acidification to coral reefs. Oceanography 26:149–152

    Article  Google Scholar 

  • Fabina NS, Putnam HM, Franklin EC et al (2013) Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral-Symbiodinium symbioses. Glob Change Biol 19:3306–3316

    Google Scholar 

  • Fast NM, Xue L, Bingham S et al (2002) Re-examining alveolate evolution using multiple protein molecular phylogenies. J Euk Microbiol 49:30–37

    Article  CAS  PubMed  Google Scholar 

  • Fay SA, Weber MX (2012) The occurrence of mixed infections of Symbiodinium (Dinoflagellata) within individual hosts. J Phycol 48:1306–1316

    Article  PubMed  Google Scholar 

  • Fensome RA, Saldarriaga JF, Taylor FJR (1999) Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies. Grana 38:66–80

    Article  Google Scholar 

  • Fitt W, Pardy R (1981) Effects of starvation, and light and dark on the energy metabolism of symbiotic and aposymbiotic sea anemones, Anthopleura elegantissima. Mar Biol 61:199–205

    Article  Google Scholar 

  • Franklin EC, Stat M, Pochon X et al (2012) 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 

  • Fransolet D, Roberty S, Plumier J-C (2012) Establishment of endosymbiosis: the case of cnidarians and Symbiodinium. J Exp Mar Biol Ecol 420–421:1–7

    Article  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 

  • Gabay Y, Benayahu Y, Fine M (2013) Does elevated pCO2 affect reef octocorals? Ecol Evol 3:465–473

    Article  PubMed  PubMed Central  Google Scholar 

  • Gleason DF, Hofmann DK (2011) Coral larvae: from gametes to recruits. J Exp Mar Biol Ecol 408:42–57

    Article  Google Scholar 

  • Godinot C, Houlbrèque F, Grover R et al (2011) Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous changes in temperature and pH. PLoS One 6, e25024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon BR, Leggat W (2010) Symbiodinium-invertebrate symbioses and the role of metabolomics. Mar Drugs 8:2546–2568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottschling M, McLean TI (2013) New home for tiny symbionts: dinophytes determined as zooxanthella are Peridiniales and distantly related to Symbiodinium. Mol Phylogenet Evol 67:217–222

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Goulet TL, Coffroth MA (1997) A within colony comparison of zooxanthella genotypes in the Caribbean gorgonian Plexaura kuna. Proceedings of the 8th international coral reef symposium 2:1331–1334

    Google Scholar 

  • Hartle-Mougiou K, D'Angelo C, Smith EG et al (2012) Diversity of zooxanthellae from corals and sea anemones after long-term aquarium culture. J Mar Biol 92:687–691

    Article  CAS  Google Scholar 

  • Hill MS (1996) Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar Biol 125:649–654

    Article  Google Scholar 

  • Hill M, Hill A (2012) The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biol Rev 87:804–821

    Article  Google Scholar 

  • Hill R, Ulstrup KE, Ralph PJ (2009) Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bull Mar Sci 85:223–244

    Google Scholar 

  • Hill M, Allenby A, Ramsby B et al (2011) Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol Phylogenet Evol 59:81–88

    Article  PubMed  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  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 

  • Howells E, Beltran V, Larsen N et al (2011) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Change 2:116–120

    Article  Google Scholar 

  • Hume B, D’Angelo C, Burt J et al (2013) Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Mar Pollut Bull 72:313–322

    Article  CAS  PubMed  Google Scholar 

  • Iglesias-Prieto R, Govind NS, Trench RK (1991) Apoprotein composition and spectroscopic characterization of the water-soluble peridinin-chlorophyll a-proteins from three symbiotic dinoflagellates. Proc R Soc Lond B 246:275–283

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikura M, Hagiwara K, Takishita K et al (2004) Isolation of new Symbiodinium strains from tridacnid giant clam (Tridacna crocea) and sea slug (Pteraeolidia ianthina) using culture medium containing giant clam tissue homogenate. Mar Biotechnol 6:378–385

    Article  CAS  PubMed  Google Scholar 

  • Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216

    Article  CAS  PubMed  Google Scholar 

  • Jeong HJ, Lee SY, Kang NS et al (2014) Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. J Euk Microbiol 61:75–94

    Article  CAS  PubMed  Google Scholar 

  • Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS One 5:e10437

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  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 

  • Kerney R (2011) Symbioses between salamander embryos and green algae. Symbiosis 54:107–117

    Article  Google Scholar 

  • Kevin MJ, Hall WT, McLaughlin JJA et al (1969) Symbiodinium microadriaticum Freudenthal, a revised taxonomic description, ultrastructure. J Phycol 5:341–350

    Article  CAS  PubMed  Google Scholar 

  • Kirk NL, Andras JP, Harvell CD et al (2009) Population structure of Symbiodinium sp. associated with the common sea fan, Gorgonia ventalina, in the Florida Keys across distance, depth, and time. Mar Biol 156:1609–1623

    Article  Google Scholar 

  • Krueger T, Gates RD (2012) Cultivating endosymbionts – host environmental mimics support the survival of Symbiodinium C15 ex hospite. J Exp Mar Biol Ecol 413:169–176

    Article  Google Scholar 

  • Kvennefors ECE, Leggat W, Hoegh-Guldberg O et al (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32:1582–1592

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS One 6:e29013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaJeunesse TC, Bhagooli R, Hidaka M et al (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, Lambert G, Andersen RA et al (2005a) Symbiodinium (Pyrrophyta) genome sizes (DNA content) are smallest among dinoflagellates. J Phycol 41:880–886

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Lee S, Bush S et al (2005b) Persistence of non-Caribbean algal symbionts in Indo-Pacific mushroom corals released to Jamaica 35 years ago. Coral Reefs 24:157–159

    Article  Google Scholar 

  • LaJeunesse TC, Pettay DT, Sampayo EM et al (2010a) 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, Smith R, Walther M et al (2010b) Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proc R Soc Lond B 277:2925–2934

    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  PubMed  Google Scholar 

  • Leggat W, Yellowlees D, Medina M (2011) Recent progress in Symbiodinium transcriptomics. J Exp Mar Biol Ecol 408:120–125

    Article  CAS  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherland, pp 405–419

    Chapter  Google Scholar 

  • Lesser M, Stat M, Gates R (2013) The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs:1–9

    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 

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

    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, Modeo L, Verni F et al (2005) Euplotes uncinatus (Ciliophora, Hypotrichia), a new species with zooxanthellae. Mar Biol 147:1055–1061

    Article  Google Scholar 

  • Logan DDK, LaFlamme AC, Weis VM et al (2010) Flow cytometric characterization of the cell-surface glycans of symbiotic dinoflagellates (Symbiodinium spp.). J Phycol 46:525–533

    Article  CAS  Google Scholar 

  • Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861

    Article  Google Scholar 

  • Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Article  Google Scholar 

  • McEwan M, Humayun R, Slamovits CH et al (2008) Nuclear genome sequence survey of the dinoflagellate Heterocapsa triquetra. J Euk Microbiol 55:530–535

    Article  CAS  PubMed  Google Scholar 

  • McGinley MP, Aschaffenburg MD, Pettay DT et al (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7

    Article  Google Scholar 

  • McGuinness DH, Dehal PK, Pleass RJ (2003) Pattern recognition molecules and innate immunity to parasites. Trends Parasitol 19:312–319

    Article  CAS  PubMed  Google Scholar 

  • Meyer E, Weis VM (2012) Study of cnidarian-algal symbiosis in the ‘omics’ age. Biol Bull 223:44–65

    CAS  PubMed  Google Scholar 

  • Mieog J, van Oppen M, Cantin N et al (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 

  • Miller DJ, Ball EE, Technau U (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet 21:536–539

    Article  CAS  PubMed  Google Scholar 

  • Moestrup O, Lindberg K, Daugbjerg N (2009) Studies on woloszynskioid dinoflagellates IV: the genus Biecheleria gen. nov. Phycol Res 57:203–220

    Article  Google Scholar 

  • Muller-Parker G (1984) Dispersal of zooxanthellae on coral reefs by predators on cnidarians. Biol Bull 167:159–167

    Article  Google Scholar 

  • Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Invert Biol 120:104–123

    Article  Google Scholar 

  • Nesa B, Baird AH, Harii S et al (2012) Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool Stud 51:12–17

    CAS  Google Scholar 

  • Noonan SHC, Fabricius KE, Humphrey C (2013) Symbiodinium community composition in scleractinian corals is not affected by life-long exposure to elevated carbon dioxide. PLoS One 8:e63985

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Norton JH, Prior HC, Baillie B et al (1995) Atrophy of the zooxanthellal tubular system in bleached giant clams Tridacna gigas. J Invertebr Pathol 66:307–310

    Article  Google Scholar 

  • Nyholm SV, McFall-Ngai M (2004) The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2:632–642

    Article  CAS  PubMed  Google Scholar 

  • Ortiz JC, González-Rivero M, Mumby PJ (2013) Can a thermally tolerant symbiont improve the future of Caribbean coral reefs? Glob Change Biol 19:273–281

    Article  Google Scholar 

  • Palumbi SR, Barshis DJ, Traylor-Knowles N et al (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898

    Article  CAS  PubMed  Google Scholar 

  • Pettay DT, LaJeunesse TC (2013) Long-range dispersal and high-latitude environments influence the population structure of a “stress-tolerant” dinoflagellate endosymbiont. PLoS One 8, e79208

    Article  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Pochon X, Pawlowski J (2006) Evolution of the soritids-Symbiodinium symbiosis. Symbiosis 42:77–88

    Google Scholar 

  • Pochon X, Putnam HM, Burki F et al (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS One 7, e29816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poland DM, Mansfield JM, Hannes AR et al (2013) Variation in Symbiodinium communities in juvenile Briareum asbestinum (Cnidaria: Octocorallia) over temporal and spatial scales. Mar Ecol Prog Ser 476:23–37

    Article  Google Scholar 

  • Ragni M, Airs RL, Hennige SJ et al (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406:57–70

    Article  CAS  Google Scholar 

  • Reynolds JM, Bruns BU, Fitt WK et al (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA 105:13674–13678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizzo PJ, Noodén LD (1972) Chromosomal proteins in the dinoflagellate alga Gyrodinium cohnii. Science 176:796–797

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rosell D, Uriz MJ (1992) Do associated zooxanthellae and the nature of the substratum affect survival, attachment and growth of Cliona viridis (Porifera: Hadromerida)? An experimental approach. Mar Biol 114:503–707

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy S, Morse D (2012) A full suite of histone and histone modifying genes are transcribed in the dinoflagellate Lingulodinium. PLoS One 7:e34340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  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, Coffroth MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis. J Phycol 37:900–912

    Article  CAS  Google Scholar 

  • Santos SR, Gutierrez-Rodriguez C, Lasker HR et al (2003) Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates. Mar Biol 143:111–120

    Article  Google Scholar 

  • Santos SR, Shearer TL, Hannes AR et al (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 

  • Schnitzler CE, Weis VM (2010) Coral larvae exhibit few measurable transcriptional changes during the onset of coral-dinoflagellate endosymbiosis. Mar Genomics 3:107–116

    Article  PubMed  Google Scholar 

  • Schnitzler C, Hollingsworth L, Krupp D et al (2012) Elevated temperature impairs onset of symbiosis and reduces survivorship in larvae of the Hawaiian coral, Fungia scutaria. Mar Biol 159:633–642

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Schönberg CHL (2006) Growth and erosion of the zooxanthellate Australian bioeroding sponge Cliona orientalis are enhanced in light. Proceedings of the 10th international coral reef symposium, Okinawa 1:168–174

    Google Scholar 

  • Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196:70–79

    Article  CAS  PubMed  Google Scholar 

  • Shinzato C, Shoguchi E, Kawashima T et al (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–323

    Article  CAS  PubMed  Google Scholar 

  • Shoguchi E, Shinzato C, Kawashima T et al (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408

    Article  CAS  PubMed  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 Lond B 279:2609–2618

    Article  Google Scholar 

  • Stat M, Gates RD (2008) Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii. Biol Invasions 10:579–583

    Article  Google Scholar 

  • 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 8:23–43

    Article  Google Scholar 

  • Stat M, Loh WKW, LaJeunesse TC et al (2009a) Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713

    Article  Google Scholar 

  • Stat M, Pochon X, Cowie ROM et al (2009b) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96

    Article  CAS  Google Scholar 

  • Stat M, Baker AC, Bourne DG et al (2012) Molecular delineation of species in the coral holobiont. Adv Mar Biol 63:1

    Article  PubMed  Google Scholar 

  • Steinke M, Brading P, Kerrison P et al (2011) Concentrations of dimethylsulfoniopropionate and dimethyl sulfide are strain-specific in symbiotic dinoflagellates (Symbiodinium sp., Dinophyceae). J Phycol 47:775–783

    Article  PubMed  Google Scholar 

  • Suggett DJ, Hall-Spencer JM, Rodolfo-Metalpa R et al (2012) Sea anemones may thrive in a high CO2 world. Glob Change Biol 18:3015–3025

    Article  Google Scholar 

  • Takabayashi M, Adams LM, Pochon X et al (2012) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai’i and Florida. Coral Reefs 31:157–167

    Article  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C et al (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teif VB, Bohinc K (2011) Condensed DNA: condensing the concepts. Prog Biophys Mol Biol 105:208–222

    Article  CAS  PubMed  Google Scholar 

  • Thornhill DJ, LaJeunesse TC, Kemp DW et al (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722

    Article  Google Scholar 

  • Thornhill DJ, Xiang Y, Fitt WK et al (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS One 4, e6262

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thornhill DJ, Xiang Y, Pettay DT et al (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 22:4499–4515

    Article  CAS  PubMed  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 

  • Udy JW, Hinde R, Vesk M (1993) Chromosomes and DNA in Symbiodinium from Australian hosts. J Phycol 29:314–320

    Article  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    Article  CAS  PubMed  Google Scholar 

  • Venn AA, Tambutté E, Holcomb M et al (2013) Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals. Proc Natl Acad Sci USA 110:1634–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vermeij GJ (2013) The evolution of molluscan photosymbioses: a critical appraisal. Biol J Linn Soc 109:497–511

    Article  Google Scholar 

  • Vidal-Dupiol J, Adjeroud M, Roger E et al (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physiol 9:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Voolstra CR, Sunagawa S, Schwarz JA et al (2009) Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium). Comp Biochem Physiol Part D Genomics Proteomics 4:67–74

    Article  PubMed  CAS  Google Scholar 

  • Wall CB, Fan T-Y, Edmunds PJ (2014) Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum. Coral Reefs 33:119–130

    Article  Google Scholar 

  • Wang J-T, Meng P-J, Chen Y-Y et al (2012) Determination of the thermal tolerance of Symbiodinium using the activation energy for inhibiting photosystem II activity. Zool Stud 51:137–142

    CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  CAS  PubMed  Google Scholar 

  • Weis VM, Allemand D (2009) What determines coral health? Science 324:1153–1155

    Article  CAS  PubMed  Google Scholar 

  • Weis VM, Davy SK, Hoegh-Guldberg O et al (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23:369–376

    Article  PubMed  Google Scholar 

  • Weisz JB, Massaro AJ, Ramsby BD et al (2010) Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biol Bull 219:189–197

    PubMed  Google Scholar 

  • Wilkerson FP, Kobayashi D, Muscatine L (1988) Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7:29–36

    Article  Google Scholar 

  • Wirshing HH, Feldheim KA, Baker AC (2013) Vectored dispersal of Symbiodinium by larvae of a Caribbean gorgonian octocoral. Mol Ecol 22:4413–4432

    Article  PubMed  Google Scholar 

  • Wisecaver JH, Hackett JD (2011) Dinoflagellate genome evolution. Annu Rev Microbiol 65:369–387

    Article  CAS  PubMed  Google Scholar 

  • Withers NW, Kokke WCMC, Fenical W et al (1982) Sterol patterns of cultured zooxanthellae isolated from marine invertebrates: synthesis of gorgosterol and 23-desmethylgorgosterol by aposymbiotic algae. Proc Natl Acad Sci USA 79:3764–3768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong JTY, New DC, Wong JCW et al (2003) Histone-like proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins. Euk Cell 2:646–650

    Article  CAS  Google Scholar 

  • Wood-Charlson EM, Weis VM (2009) The diversity of C-type lectins in the genome of a basal metazoan, Nematostella vectensis. Dev Comp Immunol 33:881–889

    Article  CAS  PubMed  Google Scholar 

  • Wood-Charlson EM, Hollingsworth LH, Krupp DA et al (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1994

    Article  CAS  PubMed  Google Scholar 

  • Yakovleva IM, Baird AH, Yamamoto HH et al (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112

    Article  CAS  Google Scholar 

  • Yamashita H, Suzuki G, Hayashibara T et al (2013) Acropora recruits harbor “rare” Symbiodinium in the environmental pool. Coral Reefs 32:355–366

    Article  Google Scholar 

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Virginia M. Weis .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kirk, N.L., Weis, V.M. (2016). Animal–Symbiodinium Symbioses: Foundations of Coral Reef Ecosystems. In: Hurst, C. (eds) The Mechanistic Benefits of Microbial Symbionts. Advances in Environmental Microbiology, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-28068-4_10

Download citation

Publish with us

Policies and ethics