Advertisement

Physiological Adaptation to Symbiosis in Cnidarians

  • Paola FurlaEmail author
  • Sophie Richier
  • Denis Allemand
Chapter

Abstract

Up to the nineteenth century, cnidarians, among other organisms such as echinoderms and sponges, were classified as zoophytes, or animal – plant. This term, initially used by Wotton in 1552 and later by Linné and Cuvier (Daudin 1926), was only referring at this time to the external shape of the organisms, fixed branched one. This term was abandoned in the twentieth century; it is however curious to note that biological and physiological reasons might support this term. Indeed, Brandt at the end of the nineteenth century showed the presence of photosynthetic algae inside the tissues of these animals. He suggested that these algae were symbiotic and called them zooxanthellae (Brandt 1881; see Perru 2003, for a review). Zooxanthellae belong to the dinoflagellate phylum and were initially considered as a single species, called Symbiodinium microadriaticum (Freudenthal 1962). It was presently shown to be highly diverse and subdivided in Symbiodinium clades (Pochon et al. 2006). Associations of these different clades with their host did not evolve randomly and members of the same cnidarian species generally harbor the same Symbiodinium clade(s) (see review by Coffroth and Santos 2005, Stambler 2010 this book).

Keywords

Endosymbiosis mutualism symbiodinium carbon concentrating mechanism carbonic anhydrase ROS superoxide dismutase catalase MAAs pocilloporins 

References

  1. Aizawa K, Miyachi S (1986) Carbonic anhydrase and CO2-concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Rev 39:215–233CrossRefGoogle Scholar
  2. Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miler DJ, Wiedenmann J, Salih A, Matz MV (2008) Diversity and evolution of coral fluorescent proteins. PLoS ONE 3:e2680CrossRefGoogle Scholar
  3. Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941CrossRefGoogle Scholar
  4. Al-Moghrabi S, Goiran C, Allemand D, Speziale N, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/ dinoflagellate association. II. Mechanisms for bicarbonate uptake. J Exp Mar Biol Ecol 199:227–248CrossRefGoogle Scholar
  5. Ambarsari I, Brown BE, Barlow RG, Britton G, 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 159:303–307CrossRefGoogle Scholar
  6. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Shifting to new algal symbionts may safeguard devastated reefs from extinction. Nature 430:CBl153CrossRefGoogle Scholar
  7. Bénazet-Tambutté S, Allemand D, Jaubert J (1996) Inorganic carbon supply to symbiont photosynthesis of the sea anemone, Anemonia viridis: role of the oral epithelial layers. Symbiosis 20:199–217Google Scholar
  8. Bentley R (1990) The shikimate pathway – a metabolic tree with many branches. Crit Rev Biochem Mol Biol 25:307–384CrossRefGoogle Scholar
  9. Bertucci A, Tambutté É, Tambutté S, Allemand D, Zoccola D (2010) Symbiosis-dependant gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H + -ATPase gene. Proc R Soc B 277:87–95CrossRefGoogle Scholar
  10. Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superioxide radicals by green fluorescent protein. Biochim Biophys Acta 1760:1690–1695Google Scholar
  11. Bowes G, Salvuci ME (1989) Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat Bot 34:233–266CrossRefGoogle Scholar
  12. Brandt K (1881) Uber das Zusammenleben von Algen und Tieren. Biologisches Centralblatt 1:524–527Google Scholar
  13. Bronstein JL (2001) The costs of mutualism. Amer Zool 41:825–839CrossRefGoogle Scholar
  14. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34CrossRefGoogle Scholar
  15. D’Aoust BG, White R, Wells JM, Olsen DA (1976) Coral-algal associations: Capacity for producing and sustaining elevated oxygen tensions in situ. Undersea Biomed Res 3:35–40Google Scholar
  16. Daudin H (1926) Cuvier et Lamarck. Les classes zoologiques et l’idée de série animale. Félix Alcan, Paris, pp 1790–1830Google Scholar
  17. Douglas AE, McAuley PJ, Davies PS (1993) Algal symbiosis in cnidarian. J Zool 231:175–178CrossRefGoogle Scholar
  18. Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116CrossRefGoogle Scholar
  19. Dove SG, Hoegh-Guldberg O, Ranganathan S (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19:197–204CrossRefGoogle Scholar
  20. Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol 112B:105–114Google Scholar
  21. Dunlap WC, Shick JM, Yamamoto Y (2000) UV protection in marine organisms. I. Sunscreens, oxidative stress and antioxidants. In: Yoshikama Y, Toyokuni S, Yamamoto Y, Naito Y (eds) Free radicals in chemistry, biology and medicine. OICA International, LondonGoogle Scholar
  22. Dykens JA, Shick JM (1982) Oxygen production by endosymbiotic algae controls superoxyde dismutase activity in their animal host. Nature 297:579–580CrossRefGoogle Scholar
  23. Dykens JA, Shick JM, Benoit C, Buettner GR, Winston GW (1992) Oxygen radical production in the sea anemone Anthopleura elegantissima and its endosymbiotic algae. J Exp Biol 168:219–241Google Scholar
  24. Edge R, McGarvey DJ, Truscott TG (1997) The carotenoids as anti-oxidants - a review. J Photochem Photobiol B 41:189–200CrossRefGoogle Scholar
  25. Fine PEM (1975) Vectors and vertical transmission: an epidemiological perspective. Ann NY Acad Sci 266:173–194Google Scholar
  26. Freudenthal HD (1962) Symbiodinium gen. nov. Symbiodinium microadriaticum sp. nov., a zooxanthella: Taxonomy, life cycle, and morphology. J Protozool 9:45–52Google Scholar
  27. Furla P, Bénazet-Tambutté S, Jaubert J, Allemand D (1998a) Functional polarity of the tentacle of the sea anemone Anemonia viridis: Role in inorganic carbon acquisition. Amer J Physiol (Regul Integr Comp Physiol) 274:R303–R310Google Scholar
  28. Furla P, Bénazet-Tambutté S, Jaubert J, Allemand D (1998b) Diffusional permeability of dissolved inorganic carbon through the isolated oral epithelial layers of the sea anemone, Anemonia viridis. J Exp Mar Biol Ecol 221:71–88CrossRefGoogle Scholar
  29. Furla P, Allemand D, Orsenigo MN (2000a) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Amer J Physiol (Regul Integr Comp) 278:R870–R881Google Scholar
  30. Furla P, Galgani I, Durand I, Allemand D (2000b) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457Google Scholar
  31. Furla P, Allemand D, Ferrier-Pages C, Shick M (2005) The symbiotic anthozoan: physiological chimera between alga and animal. Integr Comp Biol (formerly Am Zool) 45:595–604CrossRefGoogle Scholar
  32. Furla P, Richier S, Merle P-L, Garello G, Plantivaux A, Forcioli D, Allemand D (2008) Roles and origins of superoxide dismutases in a symbiotic cnidarian. In: Organisms SEaEGoCR (ed) 11th international coral reef symposium, Fort Lauderdale, 2008Google Scholar
  33. Ganot P, Moya A, Deleury E, Allemand D, Furla P, Sabourault C (2008) Exploring symbiotic interactions in the sea anemone-zooxanthellae model by large-scale ests analysis. In: Organisms SEaEGoCR (ed) 11th International coral reef symposium, Fort Lauderdale, 2008Google Scholar
  34. Gilmore AM, Larkum AWD, Salih A, Itoh S, Shibata Y, Bena C, Yamasaki H, Papina M, Van Woesik R (2003) Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem Photobiol 77:515–523CrossRefGoogle Scholar
  35. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131CrossRefGoogle Scholar
  36. Gluck S, Nelson R (1992) The role of the V-ATPase in renal epithelium H + transport. J Exp Biol 172:205–218Google Scholar
  37. Goiran C, Al-Moghrabi S, Allemand D, 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 199:207–225CrossRefGoogle Scholar
  38. Goiran C, Allemand D, Galgani I (1997) Transient Na+ stress in symbiotic dinoflagellates after isolation from coral-host cells and subsequent immersion in seawater. Mar Biol 129:581–589CrossRefGoogle Scholar
  39. Goodson MS, Whitehead F, Douglas AE (2001) Symbiotic dinoflagellates in marine cnidaria: diversity and function. Hydrobiologia 461:79–82Google Scholar
  40. Grover R, Maguer JF, Reynaud-Vaganay S, F-P C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790CrossRefGoogle Scholar
  41. Grover R, Maguer JF, Allemand D, Ferrier-Pages C (2003) Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48:2266–2274CrossRefGoogle Scholar
  42. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C (2006) Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 332:216–225CrossRefGoogle Scholar
  43. Halliwell B, Guteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  44. Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature 291:513–515CrossRefGoogle Scholar
  45. Kirschner LB (1991) Water and ions. In: Prosser CL (ed) Environmental and metabolic animal physiology. Wiley-Liss, New York, pp 13–107Google Scholar
  46. Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255CrossRefGoogle Scholar
  47. Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, Badgaer MR, Yellowlees D (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29:309–322CrossRefGoogle Scholar
  48. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperature. Coral Reefs 16:187–192CrossRefGoogle Scholar
  49. Lesser MP (2005) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–257CrossRefGoogle Scholar
  50. Lopez I, Egea R, Herrera FC (1991) Are cœlenterate cells permeable to large anions? Comp Biochem Physiol 100A:193–198CrossRefGoogle Scholar
  51. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA (1999) Fluorescent proteins from non bioluminescent Anthozoa species. Nat Biotechnol 17:969–973CrossRefGoogle Scholar
  52. Matz MV, Marshall NJ, Vorobyev M (2006) Are corals colorful? Photochem Photobiol 82:345–350CrossRefGoogle Scholar
  53. Mayfield AB, Gates RD (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp Biochem Physiol 147A:1–10Google Scholar
  54. Mazel CH, Lesser MP, Gorbunov MY, Barry TM, Farrel JH, Wyman KD, Falkowski PG (2003) Green-fluorescent proteins in Caribbean corals. Limnol Oceanogr 48:402–411CrossRefGoogle Scholar
  55. Merle PL, Sabourault C, Richier S, Allemand D, Furla P (2007) Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Radic Biol Med 42(2):236–246Google Scholar
  56. Mobley KB, Gleason DF (2003) The effect of light and heterotrophy on carotenoid concentrations in the Caribbean anemone Aiptasia pallida (Verrill). Mar Biol 143:629–637CrossRefGoogle Scholar
  57. Oswald F, Schmitt F, Leutenegger A, Ivanchenko S, D’Angelo C, Salih A, Maslakova S, Bulina M, Schirmbeck R, Nienhaus GU, Matz MV, Wiedenmann J (2007) Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J 274:1102–1109CrossRefGoogle Scholar
  58. Palmer CV, Mydlarz LD, Willis BL (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc R Soc Ser B Biol Sci 275:2687–2693CrossRefGoogle Scholar
  59. Perru O (2003) De la Société à la Symbiose: Une histoire des découvertes sur les associations chez les êtres vivants. Librairie philosophique J. Vrin. Institut de l’Institut Interdisciplinaire d’Etudes Epistémologiques, Paris, LyonGoogle Scholar
  60. Plantivaux A (2006) Adaptation aux stress oxydants chez un Cnidaire symbiotique : approche biochimique et génomique: rôle de la Cu/Zn-SOD. Ph.D. thesis. Nice-Sophia Antipolis University, FranceGoogle Scholar
  61. Plantivaux A, Furla P, Zoccola D, Garello G, Forcioli D, Richier S, Merle P-L, Tambutté É, Tambutté S, Allemand D (2004) Molecular characterization of two CuZn-superoxide dismutases in a sea anemone. Free Radic Biol Med 37:1170–1181CrossRefGoogle Scholar
  62. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30CrossRefGoogle Scholar
  63. Prescott M, Ling M, Beddoe T (2003) The 2.2 Å crystal structure of a pocilloporin pigment reveals a nonplanar chromophore conformation. Structure 11:275–284CrossRefGoogle Scholar
  64. Raven JA (1990) Sensing pH? Plant Cell Environ 13:721–729CrossRefGoogle Scholar
  65. Raven JA (2003) Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynth Res 77:155–171CrossRefGoogle Scholar
  66. Richier S (2004) Mécanismes de résistance d’une endosymbiose marine méditerranénne aux stress oxydatifs. Ph.D. thesis. Nice-Sophia Antipolis University, FranceGoogle Scholar
  67. Richier S, Merle P-L, Furla P, Pigozzi D, Sola F, Allemand D (2003) Characterization of superoxide dismutases in anoxia- and hyperoxia- tolerant symbiotic cnidarians. Biochim Biophys Acta 1621:84–91Google Scholar
  68. Richier S, Furla P, Plantivaux A, Merle P-L, Allemand D (2005) Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208:277–285CrossRefGoogle Scholar
  69. Richier S, Cottalorda J-M, Guillaume M, Fernandez C, Allemand D, Furla P (2008) Depth-dependant response to light of the reef building coral, Pocillopora verrucosa: implication of oxidative stress. J Exp Mar Biol Ecol 357:48–56Google Scholar
  70. Rodriguez-Lanetty M, Phillips WS, Weis VM (2006) Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7:1–11CrossRefGoogle Scholar
  71. Roth E, Jeon K, Stacey G (1988) Homology in endosymbiotic systems: The term symbiosome. In: Palacios RV D (ed) Molecular genetics of plant-microbe interactions. The American Phytopatological Society, St Paul, pp 220–225Google Scholar
  72. Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8:539–553CrossRefGoogle Scholar
  73. Sachs JL, Wilcox TP (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc R Soc B 273:425–429CrossRefGoogle Scholar
  74. Salih A, Hoegh-Guldberg O, Cox G (1998) Photoprotection of symbiotic dinoflagellates by fluorescent pigments in reef. In: Greenwood JG, Hall NJ (eds) Proceedings of the Australian coral ref society 75th anniversary conference, Heron Island, 1997, pp 218–230Google Scholar
  75. Sawyer SJ, Muscatine L (2001) Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 204:3443–3456Google Scholar
  76. Schlichter D, Fricke HW (1990) Coral host improves photosynthesis of endosymbiotic algae. Naturwissenschaften 77:447–450CrossRefGoogle Scholar
  77. Schwarz JA, Weis VM, Potts DC (2002) Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Mar Biol 140:471–478CrossRefGoogle Scholar
  78. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317CrossRefGoogle Scholar
  79. Seibt C, Schlichter D (2001) Compatible intracellular ion composition of the host improves carbon assimilation by Zooxanthellae in mutualistic symbioses. Naturwissenschaften 88:382–386CrossRefGoogle Scholar
  80. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461CrossRefGoogle Scholar
  81. Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262CrossRefGoogle Scholar
  82. Shick JM, Dykens JA (1985) Oxygen detoxification in algal-invertebrate symbioses from great barrier reef. Oecologia 66:33–41CrossRefGoogle Scholar
  83. Shick JM, Lesser MP, Jokiel PL (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Glob Change Biol 2:527–545CrossRefGoogle Scholar
  84. Shick JM, Romaine-Lioud S, Ferrier-Pagès C, 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 44:1667–1682CrossRefGoogle Scholar
  85. Starcevic A, Akthar S, Dunlap WC, Shick JC, Hranueli D, Cullum J, Long PF (2008) Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis, have microbial origins. Proc Natl Acad Sci 105:2533–2537CrossRefGoogle Scholar
  86. Trench RK (1987) Dinoflagellates in non-parasitic symbioses. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific Publications, Oxford, pp 530–570Google Scholar
  87. Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509–544CrossRefGoogle Scholar
  88. Venn AA, Tambutté É, Lotto S, Zoccola D, Allemand D, Tambutté S (2009) Intracellular pH in symbiotic cnidarians. Proc Natl Acad Sci 106(39):16574–17579CrossRefGoogle Scholar
  89. Wakefield TS, Kempf SC (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 200:127–143CrossRefGoogle Scholar
  90. Weis VM (1991) The induction of carbonic anhydrase in the symbiotic sea anemone Aiptasia pulchella. Biol Bull 180:496–504CrossRefGoogle Scholar
  91. Weis VM, Reynolds WS (1999) Carbonic anhydrase expression and synthesis in the sea anemone Anthopleura elegantissima are enhanced by the presence of dinoflagellate symbionts. Physiol Biochem Zool 72:307–316CrossRefGoogle Scholar
  92. Wiedenmann J, Ivanchenko S, Oswald F, Nienhaus GU (2004) Identification of GFP-like proteins in non-bioluminescent, azooxanthellate Anthozoa opens new perspectives for bioprospecting. Mar Biotechnol 6:270–277CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.UMR 7138 SAE Systématique Adaptation EvolutionUniversité de Nice-Sophia AntipolisNiceFrance
  2. 2.Laboratoire d’Océanographie de VillefrancheUMR 7093, CNRS, Université Pierre et Marie CurieVillefranche-sur-Mer CedexFrance
  3. 3.Centre Scientifique de MonacoMonacoFrance

Personalised recommendations