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Cnidarian–Dinoflagellate Symbiosis-Mediated Adaptation to Environmental Perturbations

  • Sophie Richier
  • CÉcile Sabourault
  • Christine Ferrier-Pagés
  • Pierre-Laurent Merle
  • Paola Furla
  • Denis Allemand
Chapter
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 17)

Abstract

The symbiotic relationships between corals and their phototroph dinoflagellate, Symbiodinium sp., are at the basis of the ecology of coral reefs flourishing in tropical waters. While coral reefs present a very high biological and economic value, they are presently under stress due to climate change (seawater temperature increase and acidification). In order to live together, animal hosts and their symbionts have evolved and acquired specific adaptations ranging from trophic exchange to acquisition of new mechanisms of CO2- and N-compound uptake, to hyperoxia tolerance and more. We think that these mutualistic relationships have also produced tolerance towards environmental stress.

Keywords

Photosynthetic Active Radiation Horizontal Gene Transfer Coral Species Shikimate Pathway Symbiotic State 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank the editors, the reviewers, and Christine E. Schnitzler (Department of Zoology, Oregon State University, Corvallis, USA) for their English corrections and improvements of the manuscript.

References

  1. Al-Moghrabi, S., Allemand, D. and Jaubert, J. (1993) Valine uptake by the scleractinian coral Galaxea fascicularis: characterisation and effect of light and nutritional status. J. Comp. Physiol. B 163: 355–362.CrossRefGoogle Scholar
  2. Allemand, D., Ferrier-Pagès, C., Furla, P., Houlbrèque, F., Puverel, S., Reynaud, S., Tambutté, É., Tambutté, S. and Zoccola, D. (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. C.R. Palévol. 3: 453–467.CrossRefGoogle Scholar
  3. Allemand, D., Furla, P. and Bénazet-Tambutté, S. (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can. J. Bot. 76: 925–941.Google Scholar
  4. Alscher, R.G., Erturk, N. and Heath, L.S. (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53: 1331–1341.PubMedCrossRefGoogle Scholar
  5. Ambarsari, I., Brown, B.E., Barlow, R.G., Britton, G. and Cummings, D. (1997) Fluctuations in algal chlorophyll and carotenoid pigments during solar bleaching in the coral Goniastrea aspera at Phuket, Thailand. Mar. Ecol. Prog. Ser. 159: 303–307.CrossRefGoogle Scholar
  6. Asada, K. and Takahashi, M. (1987) Production and scavenging of active oxygen in photosynthesis, In: D.J. Kyle, C.B. Osmond, and C.J. Arntzen (eds.) Photoinhibition. Elsevier, Amsterdam, pp. 227–287.Google Scholar
  7. Baker, A.C. (2001) Reef corals bleach to survive change. Nature 411: 765–766.PubMedCrossRefGoogle Scholar
  8. Baker, A.C. (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34: 661–689.CrossRefGoogle Scholar
  9. Baker, A.C. and Romanski, A.M. (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet (2006) Mar. Ecol. Prog. Ser. 335: 237–242.CrossRefGoogle Scholar
  10. Baker, A.C., Starger, C.J., McClanahan, T.R. and Glynn, P.W. (2004) Corals’ adaptive response to climate change. Nature 430: 741.PubMedCrossRefGoogle Scholar
  11. Banaszak, A.T. and Trench, R.K. (1995a) 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.CrossRefGoogle Scholar
  12. Banaszak, A.T. and Trench, R.K. (1995b) Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses – II: the synthesis of mycosporine-like amino acids in response to exposure to UV in Anthopleura elegantissima and Cassiopeia xamachana. J. Exp. Mar. Biol. Ecol. 194: 233–250.CrossRefGoogle Scholar
  13. Banaszak, A.T. and Trench, R. (2001) Ultraviolet sunscreens in dinoflagellates. Protist 152: 93–101.PubMedCrossRefGoogle Scholar
  14. Barnes, D.J. and Chalker, B.E. (1990) Calcification and photosynthesis in reef-building corals and algae, In: Z. Dubinsky (ed.) Coral Reefs. Elsevier, Amsterdam, pp. 109–131.Google Scholar
  15. Bénazet-Tambutté, S., Allemand, D. and Jaubert, J. (1996) Permeability of the oral epithelial layers in cnidarians. Mar. Biol. 126: 43–53.CrossRefGoogle Scholar
  16. Benson, A.A. and Simmons, R.E. (1981) Arsenic accumulation in Great Barrier Reef invertebrates. Science 211: 482–483.PubMedCrossRefGoogle Scholar
  17. Bentley, R. (1990) The shikimate pathway – a metabolic tree with many branches. Crit. Rev. Biochem. Mol. Biol. 25: 307–384.PubMedCrossRefGoogle Scholar
  18. Bou-Abdallah, F., Chasteen, N.D. and Lesser, M.P. (2006) Quenching of superioxide radicals by green fluorescent protein. Biochim. Biophys. Acta 1760: 1690–1695.PubMedCrossRefGoogle Scholar
  19. Brown, B.E., Ambarsari, I., Warner, M.E., Fitt, W.K., Dunne, R.P., Gibb, S.W. and Cummings, D. (1999) Diurnal changes in photochemical efficiency and xantophyll concentrations in shallow water reef corals: evidence from photoinhibition and photoprotection. Coral Reefs 18: 99–106.CrossRefGoogle Scholar
  20. Brown, B.E., Dunne, R.P., Goodson, M.S. and Douglas, A.E. (2000) Bleaching patterns in reef corals. Nature 404: 142–143.PubMedCrossRefGoogle Scholar
  21. Brown, B.E., Dunne, R.P., Goodson, M.S. and Douglas, A.E. (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21: 119–126.Google Scholar
  22. Buddemeier, R.W. and Fautin, D.G. (1993) Coral bleaching as an adaptative mechanism: a testable hypothesis. BioScience 43: 320–326.CrossRefGoogle Scholar
  23. Cairns, S.D. (1999) Species richness of recent scleractinia. Atoll Res. Bull. 459: 1–46.CrossRefGoogle Scholar
  24. Carlos, A.A., Baillie, B.K., Kawachi, M. and 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.CrossRefGoogle Scholar
  25. Coffroth, M.A. and Santos, S.R. (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156: 19–34.PubMedCrossRefGoogle Scholar
  26. Coles, S.L. and Brown, B.E. (2003) Coral bleaching – capacity for acclimatization and adaptation. Adv. Mar. Biol. 46: 183–223.PubMedCrossRefGoogle Scholar
  27. Davis, C.C. and Wurdack, K.J. (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305: 676–678.PubMedCrossRefGoogle Scholar
  28. Dove, S. (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar. Ecol. Prog. Ser. 272: 99–116.CrossRefGoogle Scholar
  29. Dove, S.G., Takabayashi, M. and Hoegh-Guldberg, O. (1995) Isolation and partial characterization of the pink and blue pigments of pocilloporid and acroporid corals. Biol. Bull. 189: 288–297.CrossRefGoogle Scholar
  30. Dove, S.G., Hoegh-Guldberg, O. and Ranganathan, S. (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19: 197–204.CrossRefGoogle Scholar
  31. Dunlap, W.C. and Yamamoto, Y. (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp. Biochem. Physiol. 112B: 105–114.Google Scholar
  32. Dunlap, W.C., Shick, J.M. and Yamamoto, Y. (2000) UV protection in marine organisms. I. Sunscreens, oxidative stress and antioxidants, In: Y. Yoshikama, S. Toyokuni, Y. Yamamoto and Y. Naito (eds.) Free Radicals in Chemistry, Biology and Medicine. OICA International, London.Google Scholar
  33. Dunning Hotopp, J.C., Clark, M.E., Oliveira, D.C.S.G., Foster, J.M, Fischer, P., Muñoz Torres, M.C., Giebel, J.D., Kumar, N., Ishmael, N., Wang, S., Ingram, J., Nene, R.V., Shepard, J., Tomkins, J., Richards, S., Spiro, D.J., Ghedin, E., Slatko, B.E., Tettelin, H. and Werren, J.H. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317: 1753–1756.PubMedCrossRefGoogle Scholar
  34. Duysens, L.N.M. and Sweers, H.E. (1963) The mechanism of two photochemical reactions in algae studied by means of fluorescence, In: Japanese Society of Plant Physiologists (eds) Studies of Microalgae and Photosynthetic Bacteria. University of Tokyo Press, Tokyo, pp. 353–372.Google Scholar
  35. Dykens, J.A. and Shick, J.M. (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297: 579–580.CrossRefGoogle Scholar
  36. Edge, R., McGarvey, D.J. and Truscott, T.G. (1997) The carotenoids as anti-oxidants – a review. J. Photochem. Photobiol. B 41: 189–200.PubMedCrossRefGoogle Scholar
  37. Fautin, D.G. and Buddemeier, R.W. (2004) Adaptative bleaching: a general phenomenon. Hydrobiologica 530/531: 459–467.CrossRefGoogle Scholar
  38. Fine, P.E.M. (1975) Vectors and vertical transmission: an epidemiological perspective. Ann. N.Y. Acad. Sci. 266: 173–194.PubMedCrossRefGoogle Scholar
  39. Ferrier-Pages, C., Richard, C., Forcioli, D., Allemand, D., Pichon, M. and Shick, J. M. (2007) Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species. Biol. Bull. 213: 76–87.PubMedCrossRefGoogle Scholar
  40. Foyer, C., Lelandais, M. and Kunert, K.J. (1994) Photoxidative stress in plants. Physiol. Plant 92: 696–717.CrossRefGoogle Scholar
  41. Freudenthal, H.D. (1962) Symbiodinium gen. nov. Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J. Protozool. 9: 45–52.Google Scholar
  42. Furla, P., Allemand, D., Ferrier-Pages, C. and Shick, M. (2005) The symbiotic anthozoan: a physiological chimera between alga and animal. Integr. Comp. Biol. 45: 595–604.PubMedCrossRefGoogle Scholar
  43. Gates, R.D. and Edmunds, P.J. (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am. Zool. 39: 30–43.Google Scholar
  44. Gattuso, J.P., Allemand, D. and Frankignoulle, M. (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am. Zool. 39: 160–183.Google Scholar
  45. Gillham, D.J. and Dodge, A.D. (1987) Chloroplast superoxide and hydrogen peroxide scavenging systems from pea leaves: seasonal variations. Plant Science 50: 105–109.CrossRefGoogle Scholar
  46. Gilmore, A.M., Larkum, A.W.D., Salih, A., Itoh, S., Shibata, Y., Bena, C., Yamasaki, H., Marina Papina M., and Van Woesik, R. (2003) Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellae chlorophyll in reef-building corals. Photochem. Photobiol. 77: 515–523.PubMedCrossRefGoogle Scholar
  47. Gladyshev, E.A., Meselson, M. and Arkhipova, I.R. (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320: 1210–1213.PubMedCrossRefGoogle Scholar
  48. Gleason, D.F. and Wellington, G.M. (1995) Variation in UVB sensivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Mar. Biol. 123: 693–703.CrossRefGoogle Scholar
  49. Glynn, P.W., Mate, J.L., Baker, A.C. and Calderon, M.O. (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Nino-Southern Oscillation event: spatial/temporal patterns and comparison with the 1982–1983 event. Bull. Mar. Sci. 69: 79–109.Google Scholar
  50. Goiran, C., Al-Moghrabi, S., Allemand, D. and Jaubert, J. (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/ dinoflagellate association. I. Photosynthetic performances of symbionts and dependence on sea water bicarbonate. J. Exp. Mar. Biol. Ecol. 199: 207–225.CrossRefGoogle Scholar
  51. Goodson, M.S., Whitehead, F. and Douglas, A.E. (2001) Symbiotic dinoflagellates in marine Cnidaria: diversity and function. Hydrobiologia 461: 79–82.CrossRefGoogle Scholar
  52. Goulet, T.L. (2006) Most corals may not change their symbionts. Mar. Ecol. Progr. Ser. 321: 1–7.CrossRefGoogle Scholar
  53. Grover, R., Maguer, J.F., Allemand, D. and Ferrier-Pagès, C. (2006) Urea uptake by the scleractinian coral Stylophora pistillata. J. Exp. Mar. Biol. Ecol. 332: 216–225.CrossRefGoogle Scholar
  54. Grover, R., Maguer, J.F., Allemand, D. and Ferrier-Pagès, C. (2003) Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol. Oceanogr. 48: 2266–2274.CrossRefGoogle Scholar
  55. Grover, R., Maguer, J.F., Reynaud-Vaganay, S. and Ferrier-Pagès, C. (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol. Oceanogr. 47: 782–790.CrossRefGoogle Scholar
  56. Haddock, S.H.D., Dunn, C.W., Philip, R.P. and Schnitzler, C. (2005) Bioluminescent and red-fluorescent lures in a deep-sea siphonophore. Science 309: 263.PubMedCrossRefGoogle Scholar
  57. Haine, E.R. (2008) Symbiont-mediated protection. Proc. R. Soc. London B 275(1633): 353–361.CrossRefGoogle Scholar
  58. Halestrap, A.P., Clarke, S.J. and Khaliulin, I. (2007) The role of mitochondria in protection of the heart by preconditioning. Biochim. Biophys. Acta 1767: 1007–1031.PubMedCrossRefGoogle Scholar
  59. Halliwell, B. and Gutteridge, J.M.C. (1999) Free radicals in biology and medicine. Oxford Science Publications.Google Scholar
  60. Harland, A.D. and Nganro, N.R. (1990) Copper uptake by the sea anemone Anemonia viridis and the role of zooxanthellae in metal regulation. Mar. Biol. 104: 297–301.CrossRefGoogle Scholar
  61. Harland, A.D., Navarro, J.C., Davies, S.P. and Fixter, L.M. (1993) Lipids of some Caribbean and Red sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar. Biol. 117: 113–117.CrossRefGoogle Scholar
  62. Hirt, R.P., Muller, S., Embley, T.M. and Coombs, G.H. (2002) The diversity and evolution of thioredoxin reductase: new perspectives. Trends Parasitol. 18: 302–308.PubMedCrossRefGoogle Scholar
  63. Hoegh-Guldberg, O. and Jones, R.J. (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar. Ecol. Progr. Ser. 183: 73–86.CrossRefGoogle Scholar
  64. Hoegh-Guldberg, O. and Salvat, B. (1995) Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Mar. Ecol. Prog. Ser. 121: 181–190.CrossRefGoogle Scholar
  65. Hoegh-Guldberg, O., Jones, R.J., Ward, S. and Loh, W.K. (2002) Is coral bleaching really adaptive? Nature 415: 601–602.PubMedCrossRefGoogle Scholar
  66. Hollingsworth, L.L., Kinzie, R.A. III, Lewis, T.D., Krupp, D.A. and Leong, J.-A.C. (2005) Phototaxis of motile zooxanthellae to green light may facilitate symbionts capture by coral larvae. Coral Reefs 24: 523.CrossRefGoogle Scholar
  67. Hoogenboom, M.O., Anthony, K.R.N. and Connolly, S.R. (2006) Energetic cost of photoinhibition in corals. Mar. Ecol. Prog. Ser. 313: 1–12.CrossRefGoogle Scholar
  68. Houlbrèque, F., Tambutté, É., Richard, C. and Ferrier-Pagès, C. (2004) Importance of the micro-diet for scleractinian corals. Mar. Ecol. Prog. Ser. 282: 151–160.CrossRefGoogle Scholar
  69. Jagger, J. (1985) Solar UV Actions On Living Cells. Praeger, New York.Google Scholar
  70. Jeffrey, S.W., MacTavish, H.S., Dunlap, W.C., Vesk, M. and Groenewould, K. (1999) Occurence of UVA- and UVB-absorbing compounds in 152 species (206 strains) of marine microalgae. Mar. Ecol. Prog. Ser. 189: 35–51.CrossRefGoogle Scholar
  71. Jimbo, M., Yanohara, T., Koike, K., Koike, K., Sakai, R., Muramoto, K. and Kamiya, H. (2000) The D-galactose-binding lectin of the octocoral Sinularia lochmodes: characterization and possible relationship to the symbiotic dinoflagellates. Comp. Biochem. Physiol. 125B: 227–236.Google Scholar
  72. Jimbo, M., Koike, K., Sakai, R., Muramoto, K. and Kamiya, H. (2005) Cloning and characterization of a lectin from the octocoral Sinularia lochmodes. Biochem. Biophys. Res. Commun. 330: 157–162.PubMedCrossRefGoogle Scholar
  73. Jokiel, P.L. and York, R.H. (1982) Solar ultraviolet photobiology of the reef coral Pocillopora damicornis and symbiotic zooxanthellae. Bull. Mar. Sci. 32: 301–315.Google Scholar
  74. Jones, R.J. and Hoegh-Guldberg, O. (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ. 24: 89–99.CrossRefGoogle Scholar
  75. Jones, R..J., Hoegh-Guldberg, O., Larkum, A.W.D. and Schreiber, U. (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21: 1219–1230.CrossRefGoogle Scholar
  76. Karntanut, W. and Pascoe, D. (2005) Effects of removing symbiotic green algae on the response of Hydra viridissima (Pallas 1776) to metals. Ecotoxicol. Environ. Safety 60: 301–305.PubMedCrossRefGoogle Scholar
  77. Kirk, N.L., Ward, R.J. and Coffroth, M.A. (2005) Stable Symbiodinium composition in the sea fan Gorgonia ventalina during temperature and disease stress. Biol. Bull. 209: 227–234.PubMedCrossRefGoogle Scholar
  78. Knowlton, N. and Rohwer, F. (2003) Multispecies microbial mutualisms on Coral Reefs: the host as a habitat. Amer. Nat. 162: S51–S62.CrossRefGoogle Scholar
  79. Koh, B. (1956) On the inhibition of photosynthesis by intense light. Biochim. Biophys. Acta 21: 234–244.CrossRefGoogle Scholar
  80. Koike, K., Jimbo, M., Sakai, R., Kaeriyama, M., Muramoto, K., Ogata, T., Maruyama, T. and Kamiya, H. (2004) Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biol Bull 207: 80–86.CrossRefGoogle Scholar
  81. Kortschak, R.D., Samuel, G., Saint, R. and Miller, D.J. (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 13: 2190–2195.PubMedCrossRefGoogle Scholar
  82. Kranner, I., Cram, W.J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., Pfeifhofer, H.W. (2005) Antioxidants and photoprotection in a lichen as compared with its isolated sym­biotic partners. Proc. Natl. Acad. Sci. U.S.A. 102: 3141–3146.PubMedCrossRefGoogle Scholar
  83. LaJeunesse, T.C. (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141: 387–400.CrossRefGoogle Scholar
  84. Leggat, W., Marendy, E.M., Baillie, B., Whitney, S.M., Ludwig, M., Badgaer, M.R. and Yellowlees, D. (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct. Plant. Biol. 29: 309–322.CrossRefGoogle Scholar
  85. Lesser, M.P. (2005) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu. Rev. Physiol. 68: 253–257.CrossRefGoogle Scholar
  86. Lesser, M.P. and Gorbunov, M.Y. (2001) Chlorophyll a fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Mar. Ecol. Prog. Ser. 212: 69–77.CrossRefGoogle Scholar
  87. Leutenegger, A., Kredel, S., Gundel, S., D’Angelo, C., Salih, A. and Wiedenmann, J. (2007) Analysis of fluorescent and non-fluorescent sea anemones from the Mediterranean Sea during a bleaching event. J. Exp. Mar. Biol. Ecol. 353: 221–234.CrossRefGoogle Scholar
  88. Levy, O., Appelbaum, L., Gothlif, Y., Hayward, D.C., Miller, D.J. and Hoegh-Guldberg, O. (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318: 467–469.PubMedCrossRefGoogle Scholar
  89. Li, C. and Jackson, R.M. (2002) Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am. J. Physiol. Cell. Physiol. 282: C227–C241.PubMedGoogle Scholar
  90. Long, S.P., Humphries, S. and Falkowski, P.G. (1994) Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Mol. Biol. 45: 633–662.CrossRefGoogle Scholar
  91. Loram, J.E., Trapido-Rosenthal, G. and Douglas, A.E. (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol. Ecol. 16: 4849–4857.PubMedCrossRefGoogle Scholar
  92. Matz, M.V., Fradkov, A.F., Labas, Y.A., Savitsky, A.P., Zaraisky, A.G., Markelov, M.L. and Lukyanov, S.A. (1999) Fluorescent proteins from non bioluminescent anthozoa species. Nat. Biotechnol. 17: 969–973.PubMedCrossRefGoogle Scholar
  93. Mayfield, A.B. and Gates, R.D. (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp. Biochem. Physiol. 147A: 1–10.Google Scholar
  94. Mazel, C.H., Lesser, M.P., Gorbunov, M.Y., Barry, T.M., Farrel, J.H., Wyman, K.D. and Falkowski, P.G. (2003) Green-fluorescent proteins in Caribbean corals. Limnol. Oceanogr. 48: 402–411.CrossRefGoogle Scholar
  95. Mieog, J.C., Van Oppen, M.J.H., Cantin, N.E., Stam, W.T. and Olsen, J.L. (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.CrossRefGoogle Scholar
  96. Mitchelmore, C.L., Ringwood, A.H. and Weis, V.M. (2003a) Differential accumulation of cadmium and changes in glutathione levels as a function of symbiotic state in the sea anemone Anthopleura elegantissima. J. Exp. Mar. Biol. Ecol. 284: 72–85.CrossRefGoogle Scholar
  97. Mitchelmore, C.L., Verde, E.A., Ringwood, A.H. and Weis, V.M. (2003b) Differential accumulation of heavy metals in the sea anemone Anthopleura elegantissima as a function of symbiotic state. Aquat. Toxicol. 64: 317–329.PubMedCrossRefGoogle Scholar
  98. Miyawaki, A. (2002) Green fluorescent protein-like proteins in reef anthozoa animals. Cell. Struct. Funct. 27: 343–347.PubMedCrossRefGoogle Scholar
  99. Mobley, K.B. and Gleason, D.F. (2003) The effect of light and heterotrophy on carotenoid concentrations in the Caribbean anemone Aiptasia pallida (Verrill). Mar. Biol. 143: 629–637.CrossRefGoogle Scholar
  100. Moran, N.A. (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl. Acad. Sci. U.S.A. 104: 8627–8633.PubMedCrossRefGoogle Scholar
  101. Mower, J.P., Stefanović, S., Young, G.J. and Palmer, J.D. (2004) Plant genetics: gene transfer from parasitic to host plants. Nature 432: 165–166.PubMedCrossRefGoogle Scholar
  102. Muko, S., Kawasaki, K. and Sakai, K. (2000) Morphological plasticity in the coral Porites sillimaniani and its adaptive significance. Bull. Mar. Sci. 66: 225–239.Google Scholar
  103. Muller-Parker, G. (1984) Photosynthesis irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar. Biol. 82: 225–232.CrossRefGoogle Scholar
  104. Muller-Parker, G. and Davy, S.K. (2001) Temperate and tropical algal-sea anemone symbioses. Invert. Biol. 120: 104–123.CrossRefGoogle Scholar
  105. Muscatine, L. (1967) Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science 156: 516–519.PubMedCrossRefGoogle Scholar
  106. Muscatine, L. (1971) Experiments on green algae coexistent with zooxanthellae in sea anemones. Pacific Sci. 25: 13–21.Google Scholar
  107. Muscatine, L. (1990) The role of symbiotic algae in carbon and energy flux in reef corals, In: Z. Dubinsky (ed.) Coral Reefs. Elsevier, Amsterdam, pp. 75–84.Google Scholar
  108. Muscatine, L., Falkowski, P.G., Porter, J.W. and Dubinsky, Z. (1984) Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc. R. Soc. Lond. B 222: 181–202.CrossRefGoogle Scholar
  109. Oliver, J.K., Chalker, B.E. and Dunlap, W.C. (1983) Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. I. Long-term growth responses of Acropora formosa (Dana 1846). J. Exp. Mar. Biol. Ecol. 73: 11–35.CrossRefGoogle Scholar
  110. Oren, A. and Gunde-Cimerman, N. (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol. Lett. 269: 1–10.PubMedCrossRefGoogle Scholar
  111. Osmond, C.B. (1994) What is photoinhibition: some insights from comparisons of sun and shade plants, In: N.R. Baker and J.R. Bowyer (eds.) Photoinhibition of photosynthesis: from molecular mechanisms to the field. BIOS Scientific Publishers, Oxford, pp. 95–110.Google Scholar
  112. Osmond, C.B. and Grace, S.C. (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J. Exp. Bot. 46: 1351–1362.CrossRefGoogle Scholar
  113. Oswald, F., Schmitt, F., Leutenegger, A., Ivanchenko, S., D’Angelo, C., Salih, A., Maslakova, S., Bulina, M., Schirmbeck, R., Nienhaus, G.U., Matz, M.V. and Wiedenmann, J. (2007) Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J. 274: 1102–1109.PubMedCrossRefGoogle Scholar
  114. Palmer, C., Bythell, J. and Willis, B. (2008) Pigmentation as part of a general immune response in scleractinians. 11th ICRS abstract book, pp. 51.Google Scholar
  115. Papina, M., Meziane, T. and van Woesik, R. (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp. Biochem. Physiol. 135B: 533–537.Google Scholar
  116. Plantivaux, A., Furla, P., Zoccola, D., Garello, G., Forcioli, D., Richier, S., Merle, P.L., Tambutté, É., Tambutté, S. and Allemand, D. (2004) Molecular characterization of two CuZn-superoxide dismutases in a sea anemone. Free Radic. Biol. Med. 37: 1170–1181.PubMedCrossRefGoogle Scholar
  117. Pochon, X., Montoya-Burgos, J.I., Stadelmann, B. and Pawlowski, J. (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phyl. Evol. 38: 20–30.CrossRefGoogle Scholar
  118. Prescott, M., Ling, M. and Beddoe, T. (2003) The 2.2 Å crytal structure of a Pocilloporin pigment reveals a nonplanar chromophore conformation. Structure 11: 275–284.PubMedCrossRefGoogle Scholar
  119. Raymond, J. and Blankenship, R.E. (2003) Horizontal gene transfer in eukaryotic algal evolution. Proc. Natl. Acad. Sci. U.S.A. 100: 7419–7420.PubMedCrossRefGoogle Scholar
  120. Redman, R.S., Sheehan, K.B., Stout, R.G., Rodriguez, R.J. and Henson, J.M. (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298: 1581.PubMedCrossRefGoogle Scholar
  121. Regoli, F., Cerrano, C., Chierici, E., Bompadre, S. and Bavestrello, G. (2000) Susceptibility to oxidative stress of the mediterranean demosponge Petrosia ficiformis: role of endosymbionts and solar irradiance. Mar. Biol. 137: 453–461.CrossRefGoogle Scholar
  122. Regoli, F., Cerrano, C., Chierici, E., Chiantore, M.C. and Bavestrello, G. (2004) Seasonal variability of prooxidant pressure and antioxydant adaptation to symbiosis in the Mediterranean demosponge Petrosia ficiformis. Mer. Ecol. Prog. Ser. 275: 129–137.CrossRefGoogle Scholar
  123. Richier, S., Furla, P., Plantivaux, A., Merle, P.L. and Allemand, D. (2005) Symbiosis-induced adaptation to oxidative stress. J. Exp. Biol. 208: 277–285.PubMedCrossRefGoogle Scholar
  124. Richier, S., Merle, P.L., Furla, P., Pigozzi, D., Sola, F. and Allemand, D. (2003) Characterization of superoxide dismutases in anoxia- and hyperoxia- tolerant symbiotic cnidarians. Biochim. Biophys. Acta 1621: 84–91.PubMedCrossRefGoogle Scholar
  125. Richier, S., Cottalorda, J.M., Guillaume, M., Fernandez, C., Allemand, D. and Furla, P. (2008) Depht-dependant response to light of the reef building coral, Pocillopora verrucosa: implication of oxidative stress. J. Exp. Mar. Biol. Ecol. 357: 48–56.CrossRefGoogle Scholar
  126. Richter, M., Ruhle, W. and Wild, A. (1990) Studies on the mechanism of photosystem II photoinhibition II: the involvement of toxic oxygen species. Photosynth. Res. 24: 237–243.CrossRefGoogle Scholar
  127. Rodriguez-Lanetty, M., Wood-Charlson, E.M., Hollingsworth, L.L., Krupp, D.A. and Weis, V.M. (2006) Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis. Mar. Biol. 149: 713–719.CrossRefGoogle Scholar
  128. Rosenberg, E., Koren, O., Reshef, L., Efrony, R. and Zilber-Rosenberg, I. (2007) The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5: 355–362.PubMedCrossRefGoogle Scholar
  129. Rowan, R. (2004) Thermal adaptation in reef coral symbionts. Nature 430: 742.PubMedCrossRefGoogle Scholar
  130. Rowan, R. and Knowlton, N. (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 92: 2850–2853.PubMedCrossRefGoogle Scholar
  131. Rowan, R., Knowlton, N., Baker, A. and Jara, J. (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388: 265–269.PubMedCrossRefGoogle Scholar
  132. Sachs, J.L. and Wilcox, T.P. 2006. A shift to parasitism in the jellyfish symbiont Symbiodinium microadriadicum. Proc. R. Soc. B 273: 425–429.PubMedCrossRefGoogle Scholar
  133. Salih, A., Hoegh-Guldberg, O. and Cox, G. (1998) Photoprotection of symbiotic dinoflagellates by fluorescent pigments in reef corals, In: J.G. Greenwood and N.J. Hall (eds.) Proc. of Australian Coral Reef Society, 75th Anniversary Conference. pp. 218–230.Google Scholar
  134. Salih, A., Larkum, A., Cox, G., Kühl, M. and Hoegh-Guldberg, O. (2000) Fluorescent pigments in corals are photoprotective. Nature 408: 850–853.PubMedCrossRefGoogle Scholar
  135. Schlichter, D. and Fricke, H.W. (1990) Coral host improves photosynthesis of endosymbiotic algae. Naturwissenschaften 77: 447–450.CrossRefGoogle Scholar
  136. Schnitzler, E.C., Keenan, R.J., McCord, R., Matysik, A., Christianson L.M. and Haddock, S.H.D. 2008. Spectral diversity of fluorescent proteins from the anthozoan Corynactis californica. Mar. Biotechnol. 10: 328–342.PubMedCrossRefGoogle Scholar
  137. Schreiber, U. and Bilger, W. (1987) Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements, In: J.D. Tenhunen (ed.) Plant Responses to Stress. Springer, Berlin.Google Scholar
  138. Schwarz, J.A., Weis, V.M. and Potts, D.C. (2002) Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Mar. Biol. 140: 471–478.CrossRefGoogle Scholar
  139. Sebens, K.P., Vandersall, K.S., Savina, L.A. and Graham, K.R. (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar. Biol. 127: 303–317.CrossRefGoogle Scholar
  140. Shashar, N., Cohen, Y. and Loya, Y. (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol. Bull. 185: 455–461.CrossRefGoogle Scholar
  141. Shick, J.M. and Dunlap, W.C. (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 64: 223–262.PubMedCrossRefGoogle Scholar
  142. Shick, J.M. and Dykens, J.A. (1985) Oxygen detoxification in algal-invertebrate symbioses from Great Barrier reef. Oecologia 66: 33–41.CrossRefGoogle Scholar
  143. Shick, J.M., Lesser, M.P. and Stochaj, W.R. (1991) Ultraviolet radiation and photooxydative stress in zooxabthellate anthozoa: the sea anemone Phyllodiscus semoni and the Octocoral Clavularia sp. Symbiosis 10: 145–173.Google Scholar
  144. Shick, J. M., Lesser, M.P., Dunlap, W.C., Stochaj, W.R., Chalker, B.E. and Wu Won, J. (1995) Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar. Biol. 122: 41–51.CrossRefGoogle Scholar
  145. Shick, J.M., Lesser, M.P. and Jokiel, P.L. (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biol. 2: 527–545.CrossRefGoogle Scholar
  146. Shick, J.M., Romaine-Lioud, S., Ferrier-Pagès, C. and Gattuso, J.P. (1999) Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol. Oceanogr. 44: 1667–1682.CrossRefGoogle Scholar
  147. Shick, J.M., Dunlap, W.C. and Buettner, G.R. (2000) UV protection in marine organisms. II.Biosynthesis, accumulation and sunscreening function of mycosporine-like amino acids, In: Y. Yoshikama, S. Toyokuni, Y. Yamamoto and Y. Naito (eds.) Free Radicals in Chemistry, Biology and Medicine. OICA International, London.Google Scholar
  148. Shick, J.M., Dunlap, W.C., Pearse, J.S. and Pearse, V.B. (2002) Mycosporine-like amino acid content in four species of sea anemones in the genus Anthopleura reflects phylogenetic but not environmental or symbiotic relationships. Biol. Bull. 203: 315–330.PubMedCrossRefGoogle Scholar
  149. Shick, J.M., Ferrier-Pagès, C., Grover, R. and Allemand, D. (2005) Effects of starvation, ammonium concentration, and photosynthesis on the UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Mar. Ecol. Prog. Ser. 295: 135–156.CrossRefGoogle Scholar
  150. Simonson, A.B., Servin, J.A., Skophammer, R.G., Herbold, C.W., Rivera, M.C. and Lake, J.A. (2005) Decoding the genomic tree of life. Proc. Natl. Acad. Sci. U.S.A. 102: 6608–6613.PubMedCrossRefGoogle Scholar
  151. Starcevic, A., Akthar, S., Dunlap, W.C., Shick, J.C., Hranueli, D., Cullum, J. and Long, P.F. (2008) Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis, have microbial origins. Proc. Natl. Acad. Sci. U.S.A. 105: 2533–2537.PubMedCrossRefGoogle Scholar
  152. Stat, M., Morris, E., Gates, R.D. (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc. Natl. Acad. Sci. USA 15: 9256–9261CrossRefGoogle Scholar
  153. Steele, R.E., Hampson, S.E., Stover, N.A., Kibler, D.F. and Bode, H.R. (2004) Probable horizontal transfer of a gene between a protist and a cnidarian. Curr. Biol. 14: R298–R299.PubMedCrossRefGoogle Scholar
  154. Stochaj, W.R., Dunlap, W.C. and Shick, J.M. (1994) Two new UV-absorbing mycosporine-like amino acids from the sea anemone Anthopleura elegantissima and the effects if zooxanthellae and spectral irradiance on chemical composition and content. Mar. Biol. 118: 149–156.CrossRefGoogle Scholar
  155. Tchernov, D., Gorbunov, M.Y., de Vargas, C., Yadav, S.N., Milligan, A.J., Häggblom, M. and Falkowski, P.G. (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching corals. Proc. Natl. Acad. Sci. U.S.A. 101: 13531–13535.PubMedCrossRefGoogle Scholar
  156. Teai, T., Drollet, J.H., Bianchini, J.P., Cambon, A. and Martin, P.M.V. (1998) Occurrence of ultraviolet radiation-absorbing mycosporine-like amino acids in coral mucus and whole corals of French Polynesia. Marine Freshwater Res. 49: 127–132.CrossRefGoogle Scholar
  157. Technau, U., Rudd, S., Maxwell, P., Gordon, P.M.K., Saina, M., Grasso, L.C., Hayward, D.C., Sensen, C.W., Saint, R., Holstein, T.W., Ball, E.E. and Miller, D.J. (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Gen. 21: 633–639.CrossRefGoogle Scholar
  158. Telfer, A. and Barber, J. (1994) Elucidating the molecular mechanisms of photoinhibition by studying isolated photosystem II reaction centres, In: N.R. Baker and J.R. Bowyer (eds.) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. BIOS Scientific Publishers, Oxford, pp. 25–50.Google Scholar
  159. Timmis, J.N., Ayliffe, M.A., Huang, C.Y. and Martin, W. (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Rev. 5: 123–136.CrossRefGoogle Scholar
  160. Titlyanov, E.A. (1991) Light adaptation and production characteristics of branches differing by age and illumination of the hermatypic coral Pocillopora verrucosa. Symbiosis 10: 249–260.Google Scholar
  161. Tsien, R.Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67: 509–544.PubMedCrossRefGoogle Scholar
  162. Van den Hoek, T.L., Becker, L.B., Shao, Z., Li, C. and Schumacker, P. T. (1998) Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J. Biol. Chem. 273: 18092–18098.CrossRefGoogle Scholar
  163. Venn, A.A., Loram, J.E. and Douglas, A.E. (2008) Photosynthetic symbioses in animals. J. Exp. Bot. 59: 1069–1080.PubMedCrossRefGoogle Scholar
  164. Verde, E.A. and McCloskey, L.R. (2002) A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt). Mar. Biol. 141: 225–239.CrossRefGoogle Scholar
  165. Wakefield, T.S. and Kempf, S.C. (2001) Development of host- and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biol. Bull. 200: 127–143.CrossRefGoogle Scholar
  166. Walker, D. (1992) Tansely Review no. 36. Excited Leaves. New Phytol. 121: 325–345.CrossRefGoogle Scholar
  167. Wiedenmann, J., Ivanchenko, S., Oswald, F. and Nienhaus, G.U. (2004) Identification of GFP-like proteins in non-bioluminescent, azooxanthellate anthozoa opens new perspectives for bioprospecting. Mar. Biotechnol. 6: 270–277.PubMedCrossRefGoogle Scholar
  168. Willmer, P., Stone, G. and Johnston, I. (2000) Environmental Physiology of Animals. Blackwell, Oxford.Google Scholar
  169. Winters, G., Loya, Y., Roettgers, R. and Beer, S. (2003) Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnol. Oceanogr. 48: 1388–1393.CrossRefGoogle Scholar
  170. Wood-Charlson, E.M., Hollingsworth, L.L., Krupp, D.A. and Weis, V.M. (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell. Microbiol. 8: 1985–1993.PubMedCrossRefGoogle Scholar
  171. Yakovleva, I., Bhagooli, R., Takemura, A. and Hidaka, M. (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp. Biochem. Physiol. 139B: 721–730.Google Scholar
  172. Yamashiro, H., Oku, H., Higa, H., Chinen, I. and Sakai, K. (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp. Biochem. Physiol. 122B: 397–407.Google Scholar
  173. Yamashiro, H., Oku, H. and Onaga K. (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish. Sci. 71: 448–453.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Sophie Richier
    • 1
    • 2
  • CÉcile Sabourault
    • 1
  • Christine Ferrier-Pagés
    • 3
  • Pierre-Laurent Merle
    • 1
  • Paola Furla
    • 1
  • Denis Allemand
    • 3
  1. 1.Equipe Symbiose Marine, UMR 7138 UNS-UPMC-CNRS, “Systématique, Adaptation, Evolution”Universite de Nice-Sophia Antipolis, Faculté des SciencesNice Cedex 2France
  2. 2.Ocean Biogeochemistry and Ecosystem, National Oceanography Centre SouthamptonUniversity of Southampton Waterfront campusSouthamptonUnited Kingdom
  3. 3.Centre Scientifique de MonacoMonacoPrincipality of Monaco

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