Coral Reefs

, Volume 33, Issue 2, pp 501–512 | Cite as

Thermal responses of Symbiodinium photosynthetic carbon assimilation

  • Clinton A. Oakley
  • Gregory W. Schmidt
  • Brian M. HopkinsonEmail author


The symbiosis between hermatypic corals and their dinoflagellate endosymbionts, genus Symbiodinium, is based on carbon exchange. This symbiosis is disrupted by thermally induced coral bleaching, a stress response in which the coral host expels its algal symbionts as they become physiologically impaired. The disruption of the dissolved inorganic carbon (DIC) supply or the thermal inactivation of Rubisco have been proposed as sites of initial thermal damage that leads to the bleaching response. Symbiodinium possesses a highly unusual Form II ribulose bisphosphate carboxylase/oxygenase (Rubisco), which exhibits a lower CO2:O2 specificity and may be more thermally unstable than the Form I Rubiscos of other algae and land plants. Components of the CO2 concentrating mechanism (CCM), which supplies inorganic carbon for photosynthesis, may also be temperature sensitive. Here, we examine the ability of four cultured Symbiodinium strains to acquire and fix DIC across a temperature gradient. Surprisingly, the half-saturation constant of photosynthesis with respect to DIC concentration (K P), an index of CCM function, declined with increasing temperature in three of the four strains, indicating a greater potential for photosynthetic carbon acquisition at elevated temperatures. In the fourth strain, there was no effect of temperature on K P. Finding no evidence for thermal inhibition of the CCM, we conclude that CCM components are not likely to be the primary sites of thermal damage. Reduced photosynthetic quantum yields, a hallmark of thermal bleaching, were observed at low DIC concentrations, leaving open the possibility that reduced inorganic carbon availability is involved in bleaching.


Carbon limitation Coral bleaching Photosynthesis Thermal stress Symbiodinium 



We thank the laboratory of Scott Santos and Mark Warner for Symbiodinium cultures, as well as John Parkinson and the laboratory of Todd LaJeunesse for assistance in their genotypic identification. This work was developed under STAR Fellowship Assistance Agreement no. FP91719701-0 (C.A.O.) awarded by the US Environmental Protection Agency (EPA) and by a grant from the National Science Foundation (NSF EF-1041034, B.H.). It has not been formally reviewed by the EPA, and the views expressed in this work are solely those of the authors.


  1. Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941Google Scholar
  2. Al-Moghrabi S, Goiran C, Allemand D, Speziale N (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanisms for bicarbonate uptake. Mar Biol 199:227–248CrossRefGoogle Scholar
  3. Asada K (1999) The water–water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol 50:601–639CrossRefGoogle Scholar
  4. Badger MR, Palmavist K, Yu JW (1994) Measurement of CO2 and HCO3 fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol Plant 90:529–536CrossRefGoogle Scholar
  5. Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc Lond B 355:1433–1446CrossRefGoogle Scholar
  6. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76:1052–1071Google Scholar
  7. Berkelmans R, van Oppen JH (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 Biol Sci Ser B 273:2305–2312CrossRefGoogle Scholar
  8. Brooks A, Farquhar G (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165:397–406PubMedCrossRefGoogle Scholar
  9. Buxton L, Badger M, Ralph P (2009) Effects of moderate heat stress and dissolved inorganic carbon concentration on photosynthesis and respiration of Symbiodinium sp. (Dinophyceae) in culture and in symbiosis. J Phycol 45:357–365CrossRefGoogle Scholar
  10. Buxton L, Takahashi S, Hill R, Ralph PJ (2012) Variability in the primary site of photosynthetic damage in Symbiodinium sp. (Dinophyceae) exposed to thermal stress. J Phycol 48:117–126CrossRefGoogle Scholar
  11. Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457PubMedGoogle Scholar
  12. 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
  13. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195CrossRefGoogle Scholar
  14. Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98CrossRefGoogle Scholar
  15. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  16. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards a J, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–42Google Scholar
  17. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305PubMedCentralPubMedCrossRefGoogle Scholar
  18. Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond B 271:1757–1763CrossRefGoogle Scholar
  19. IPCC (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, SwitzerlandGoogle Scholar
  20. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  21. Kaplan A, Badger MR, Berry JA (1980) Photosynthesis and the intracellular inorganic carbon pool in the bluegreen alga Anabaena variabilis: Response to external CO2 concentration. Planta 149:219–226PubMedCrossRefGoogle Scholar
  22. Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: Where do we draw the line? Am Zool 39:146–159Google Scholar
  23. Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665CrossRefGoogle Scholar
  24. Kolber Z, Prasil O, Falkowski P (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106PubMedCrossRefGoogle Scholar
  25. Kuhl M, Cohen Y, Dalsgaard T, Jergensenl BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied pH and light with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172CrossRefGoogle Scholar
  26. LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581PubMedCrossRefGoogle Scholar
  27. 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 48:1380–1391CrossRefGoogle Scholar
  28. Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255PubMedCentralPubMedCrossRefGoogle Scholar
  29. Leggat W, Whitney S, Yellowlees D (2004) Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37:1–17Google Scholar
  30. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192CrossRefGoogle Scholar
  31. Lilley RM, Ralph PJ, Larkum AWD (2010) The determination of activity of the enzyme Rubisco in cell extracts of the dinoflagellate alga Symbiodinium sp. by manganese chemiluminescence and its response to short-term thermal stress of the alga. Plant Cell Environ 33:995–1004PubMedCrossRefGoogle Scholar
  32. McCabe Reynolds J, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA 105:13674–13678CrossRefGoogle Scholar
  33. Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6:1251–1259PubMedCentralPubMedCrossRefGoogle Scholar
  34. Muller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedCentralPubMedCrossRefGoogle Scholar
  35. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  36. Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci 3:291–315CrossRefGoogle Scholar
  37. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579CrossRefGoogle Scholar
  38. Rost B, Riebesell U, Burkhardt S, Sultemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67CrossRefGoogle Scholar
  39. Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53:609–620PubMedCrossRefGoogle Scholar
  40. Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217PubMedCrossRefGoogle Scholar
  41. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408PubMedCrossRefGoogle Scholar
  42. Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biol 11:1–11CrossRefGoogle Scholar
  43. Takahashi S, Whitney S, Itoh S, Maruyama T, Badger M (2008) Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium. Proc Natl Acad Sci USA 105:4203–4208PubMedCentralPubMedCrossRefGoogle Scholar
  44. Tcherkez G, Farquhar G, Andrews T (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103:7246–7251PubMedCentralPubMedCrossRefGoogle Scholar
  45. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Hagglbom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535PubMedCentralPubMedCrossRefGoogle Scholar
  46. Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 22:4499–4515PubMedCrossRefGoogle Scholar
  47. Tortell PD, Rau GH, Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45:1485–1500CrossRefGoogle Scholar
  48. Vance P, Spalding MH (2005) Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states. Can J Bot 83:796–809CrossRefGoogle Scholar
  49. Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ 19:291–299CrossRefGoogle Scholar
  50. Warner M, Fitt W, Schmidt G (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012PubMedCentralPubMedCrossRefGoogle Scholar
  51. Whitney SM, Shaw DC, Yellowlees D (1995) Evidence that some dinoflagellates contain a ribulose-1, 5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proc R Soc Lond B 259:271–275CrossRefGoogle Scholar
  52. Wooldridge SA (2009) A new conceptual model for the warm-water breakdown of the coral–algae endosymbiosis. Mar Freshw Res 60:483–496CrossRefGoogle Scholar
  53. Zahl P, McLaughlin J (1957) Isolation and cultivation of zooxanthellae. Nature 180:199–200CrossRefGoogle Scholar
  54. Zhang H, Byrne RH (1996) Spectrophotometric pH measurements of surface seawater at in situ conditions: absorbance and protonation behavior of thymol blue. Mar Chem 52:17–25CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Clinton A. Oakley
    • 1
  • Gregory W. Schmidt
    • 1
  • Brian M. Hopkinson
    • 2
    Email author
  1. 1.Department of Plant BiologyUniversity of GeorgiaAthensUSA
  2. 2.Department of Marine SciencesUniversity of GeorgiaAthensUSA

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