Thermal responses of Symbiodinium photosynthetic carbon assimilation

Coral Reefs

Volumn 33, Issue 2, 2014, Pages 501-512

  Oakley, Clinton A ^a   Schmidt, Gregory W ^a   Hopkinson, Brian M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Carbon limitation; Coral bleaching; Photosynthesis; Symbiodinium; Thermal stress

Indexed keywords

CARBON SEQUESTRATION; CORAL BLEACHING; DINOFLAGELLATE; DISSOLVED INORGANIC CARBON; ENDOSYMBIONT; ENZYME ACTIVITY; NUTRIENT AVAILABILITY; PHOTOSYNTHESIS; SYMBIOSIS; TEMPERATURE EFFECT; TEMPERATURE GRADIENT;

ALGAE; ANTHOZOA; DINOPHYCEAE; EMBRYOPHYTA; SYMBIODINIUM;

EID: 84900826707     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-014-1130-9     Document Type: Article

References (54)

1. Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76: 925-941.
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: 227-248.
3. Asada K (1999) The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol 50: 601-639.
4. - fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol Plant 90: 529-536.
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: 1433-1446.
6. 2-concentrating mechanisms in algae. Can J Bot 76: 1052-1071.
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: 2305-2312.
8. 2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165: 397-406.
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: 357-365.
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: 117-126.
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: 3445-3457.
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: 207-225.
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: 179-195.
14. Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44: 91-98.
15. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshw Res 50: 839-866.
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: 1737-42.
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: 10302-10305.
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: 1757-1763.
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, Switzerland.
20. 2 fixation mechanism in zooxanthellae. Plant Cell Environ 21: 1219-1230.
21. 2 concentration. Planta 149: 219-226.
22. Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: Where do we draw the line? Am Zool 39: 146-159.
23. Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38: 1646-1665.
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: 88-106.
25. 2, pH and light. Mar Ecol Prog Ser 117: 159-172.
26. LaJeunesse TC (2005) "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22: 570-581.
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: 1380-1391.
28. Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121: 1247-1255.
29. Leggat W, Whitney S, Yellowlees D (2004) Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37: 1-17.
30. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16: 187-192.
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: 995-1004.
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: 13674-13678.
33. Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6: 1251-1259.
34. Muller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566.
35. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27: 454-460.
36. Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci 3: 291-315.
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: 568-579.
38. Rost B, Riebesell U, Burkhardt S, Sultemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48: 55-67.
39. cat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53: 609-620.
40. Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58: 199-217.
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: 1399-1408.
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: 1-11.
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: 4203-4208.
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: 7246-7251.
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: 13531-13535.
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: 4499-4515.
47. Tortell PD, Rau GH, Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45: 1485-1500.
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: 796-809.
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: 291-299.
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: 8007-8012.
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: 271-275.
52. Wooldridge SA (2009) A new conceptual model for the warm-water breakdown of the coral-algae endosymbiosis. Mar Freshw Res 60: 483-496.
53. Zahl P, McLaughlin J (1957) Isolation and cultivation of zooxanthellae. Nature 180: 199-200.
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: 17-25.