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Thermal responses of Symbiodinium photosynthetic carbon assimilation

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Abstract

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.

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References

  • Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Badger MR, Palmavist K, Yu JW (1994) Measurement of CO2 and HCO3 fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol Plant 90:529–536

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 76:1052–1071

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 165:397–406

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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 21:1219–1230

    Article  CAS  Google Scholar 

  • 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 149:219–226

    Article  CAS  PubMed  Google Scholar 

  • Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: Where do we draw the line? Am Zool 39:146–159

    Google Scholar 

  • Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 117:159–172

    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, 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  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leggat W, Whitney S, Yellowlees D (2004) Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37:1–17

    Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6:1251–1259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Muller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Article  Google Scholar 

  • Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci 3:291–315

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rost B, Riebesell U, Burkhardt S, Sultemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67

    Article  Google Scholar 

  • 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 53:609–620

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tortell PD, Rau GH, Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45:1485–1500

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wooldridge SA (2009) A new conceptual model for the warm-water breakdown of the coral–algae endosymbiosis. Mar Freshw Res 60:483–496

    Article  CAS  Google Scholar 

  • Zahl P, McLaughlin J (1957) Isolation and cultivation of zooxanthellae. Nature 180:199–200

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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Acknowledgments

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.

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Correspondence to Brian M. Hopkinson.

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Communicated by Biology Editor Anastazia Banaszak

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Oakley, C.A., Schmidt, G.W. & Hopkinson, B.M. Thermal responses of Symbiodinium photosynthetic carbon assimilation. Coral Reefs 33, 501–512 (2014). https://doi.org/10.1007/s00338-014-1130-9

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