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Sensitivity to oxidative stress is not a definite predictor of thermal sensitivity in symbiotic dinoflagellates

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Abstract

Coral bleaching, the loss of symbiotic dinoflagellate algae (genus Symbiodinium) and/or photosynthetic algal pigments from corals, is thought to be primarily triggered by the thermal dysfunction of photosynthesis and a consequent build-up of reactive oxygen species. However, different corals exhibit differential bleaching susceptibilities, perhaps resulting from dissimilar abilities to deal with oxidative stress. We therefore tested whether thermal sensitivity in Symbiodinium is correlated with the capacity to deal with oxidative stress, by comparing the effects of increased temperature and hydrogen peroxide (H2O2) concentration on the photosynthetic performance of four cultured Symbiodinium ITS2 types (A1, B2, E, and F1) and two freshly isolated Symbiodinium ITS2 types (a temperate A-type and B1). Generally, the maximum quantum yield of photosystem II (F v/F m) declined in Symbiodinium with both increasing thermal and oxidative stress. However, not all types followed this pattern. Cultured Symbiodinium A1 showed a strong negative response to elevated temperature but little response to the addition of H2O2, while cultured F1 showed an increase in F v/F m at elevated temperature but a decline in this parameter to almost zero at high H2O2 concentrations. Furthermore, both freshly isolated Symbiodinium types appeared to be relatively stress tolerant, with the temperate A-type showing an especially high resistance to both stressors. In conclusion, a range of Symbiodinium types were shown to differ in their susceptibilities to both thermal and oxidative stress, though in contrast to our original hypothesis, sensitivity to oxidative stress did not necessarily predict thermal sensitivity (or vice versa).

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References

  • Abrego D, Ulstrup KE, Willis BL, Van Oppen MJH (2008) Species–specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond B Biol Sci 275:2273–2282

    Article  CAS  Google Scholar 

  • Ainsworth TD, Hoegh-Guldberg O, Heron SF, Skirving WJ, Leggat W (2008) Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. J Exp Mar Biol Ecol 364:63–71

    Article  Google Scholar 

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24(1):16–20

    Article  Google Scholar 

  • Bingham BL, Freytes I, Emery M, Dimond J, Muller-Parker G (2011) Aerial exposure and body temperature of the intertidal sea anemone Anthopleura elegantissima. Invertebr Biol 130(4):291–301

    Article  Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    Article  CAS  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) The cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76(2):229–261

    Article  CAS  Google Scholar 

  • Díaz-Almeyda E, Thomé PE, El Hafidi M, Iglesias-Prieto R (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30:217–225

    Article  Google Scholar 

  • Douglas AE (2003) Coral bleaching—how and why? Mar Poll Bull 46:385–392

    Article  CAS  Google Scholar 

  • Dove S, Ortiz JC, Enriquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51(2):1149–1158

    Article  Google Scholar 

  • Downs CA, McDougall KE, Woodley CM, Fauth JE, Richmond RH, Kushmaro A, Gibb SW, Loya Y, Ostrander GK, Kramarsky-Winter E (2013) Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching. PLoS ONE 8:e77173

    Article  CAS  Google Scholar 

  • Fisher PL (2006) Investigating the photo-physiology of Symbiodinium sub-clades and its relationship to coral bleaching. Ph.D. thesis, University of Queensland

  • Fisher PL, Malme MK, Dove S (2012) The effect of temperature stress on coral–Symbiodinium associations containing distinct symbiont types. Coral Reefs 31:473–485

    Article  Google Scholar 

  • Fitt WK (2000) Cellular growth of host and symbiont in a cnidarian—zooxanthellar symbiosis. Biol Bull 198:110–120

    Article  CAS  Google Scholar 

  • Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

    Article  Google Scholar 

  • Frade PR, Englebert N, Faria J, Visser PM, Bak RPM (2008) Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27:913–925

    Article  Google Scholar 

  • Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic Cnidarians: implications for coral bleaching. Biol Bull 182:324–332

    Article  Google Scholar 

  • Hawkins T, Davy SK (2012) Nitric oxide production and tolerance differ among Symbiodinium types exposed to heat stress. Plant Cell Physiol 53:1889–1898

    Article  CAS  Google Scholar 

  • Hawkins TD, Bradley BJ, Davy SK (2013) Nitric oxide mediates coral bleaching through an apoptotic-like cell death pathway: evidence from a model sea anemone-dinoflagellate symbiosis. FASEB J 27:4790–4798

    Article  CAS  Google Scholar 

  • Hawkins TD, Krueger T, Becker S, Fisher PL, Davy SK (2014) Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals. Coral Reefs 33:141–153

    Article  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 

  • Higuchi T, Fujimura H, Arakaki T, Oomori T (2008) Activities of antioxidant enzymes (SOD and CAT) in the coral Galaxea fascicularis against increased hydrogen peroxide concentrations in seawater. Proceedings of 11th international coral reef symposium, Ft. Lauderdale, Florida, pp 926–930

  • Hill R, Ralph PJ (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 352:137–144

    Article  Google Scholar 

  • Hill R, Schreiber U, Gademann R, Larkum AWD, Kühl M, Ralph PJ (2004) Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching conditions in three species of corals. Mar Biol 144:633–640

    Article  Google Scholar 

  • Hill R, Frankart C, Ralph PJ (2005) Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. J Exp Mar Biol Ecol 322:83–92

    Article  CAS  Google Scholar 

  • Hill R, Brown CM, DeZeeuw K, Campbell DA, Ralph PJ (2011) Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation. Limnol Oceanogr 56:139–146

    Article  Google Scholar 

  • Hill R, Szabó M, Rehman A, Vass I, Ralph PJ, Larkum AWD (2014) Inhibition of photosynthetic CO2 fixation in the coral Pocillopora damicornis and its relationship to thermal bleaching. J Exp Biol 217:2150–2162

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, 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 318:1737–1742

    Article  CAS  Google Scholar 

  • Howe JN (2013) The genetic and physiological characteristics of the Symbiodinium spp. in the endemic anemone Anthopleura aureoradiata. MSc thesis, Victoria University of Wellington

  • Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Change 2:116–120

    Article  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  Google Scholar 

  • Iglesias-Prieto R, Beltrán 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 Biol Sci 271:1757–1763

    Article  CAS  Google Scholar 

  • Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, Kim HS, Yih W, Yamashita H, LaJeunesse TC (2014) Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n.sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. J Eukar Microbiol 61:75–94

    Article  CAS  Google Scholar 

  • 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 

  • Jones RJ, Ward S, Amri AY, Hoegh-Guldberg O (2000) Changes in quantum efficiency of photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event. Mar Freshw Res 51:63–71

    Article  Google Scholar 

  • Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

    Article  CAS  Google Scholar 

  • Krueger T, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Fisher PL, Davy SK (2014) Antioxidant plasticity and thermal sensitivity in four types of Symbiodinium sp. J Phycol 50:1035–1047

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800

    Article  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41(2):271–283

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and Physiological Ecology. Ann Rev Physiol 68:253–278

    Article  CAS  Google Scholar 

  • Lesser MP (2011) Coral bleaching: Causes and Mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Heidelberg, pp 405–419

    Chapter  Google Scholar 

  • Lesser MP, Shick JM (1989) Photoadaption and defenses against oxygen toxicity in zooxanthellae from natural populations of symbiotic cnidarians. J Exp Mar Biol Ecol 134:129–141

    Article  Google Scholar 

  • Lilley McC R, 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  Google Scholar 

  • Logan DDK, LaFlamme AC, Weis VM, Davy SK (2010) Flow-cytometric characterization of the cell-surface glycans of symbiotic dinoflagellates (Symbiodinium spp.). J Phycol 46:525–533

    Article  CAS  Google Scholar 

  • Lough JM, Van Oppen MJH (2009) Introduction: coral bleaching—patterns, processes, causes and consequences. In: Van Oppen MJH, Lough JM (eds) coral bleaching. Springer, Berlin, pp 1–5

    Chapter  Google Scholar 

  • Marutani Y, Yamauchi Y, Kimura Y, Mizutani M, Sugimoto Y (2012) Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. Planta. doi:10.1007/s00425-012-1647-5

  • McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Invertebr Biol 120:104–123

    Article  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  Google Scholar 

  • Perez S, Weis V (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209:2804–2810

    Article  CAS  Google Scholar 

  • Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    Article  CAS  Google Scholar 

  • Pontasch S, Hill R, Deschaseaux E, Fisher PL, Davy SK, Scott A (2014) Photochemical efficiency and antioxidant capacity in relation to Symbiodinium genotype and host phenotype in a symbiotic cnidarian. Mar Ecol Prog Ser 516:195–208

    Article  CAS  Google Scholar 

  • Ralph PJ, Gademann R, Larkum AWD, Kühl M (2002) Spatial heterogeneity in active chlorophyll fluorescence and PSII activity of coral tissues. Mar Biol 141:639–646

    Article  CAS  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 

  • Roth MS (2014) The engine of the reef: photobiology of the coral–algal symbiosis. Front Microbiol 5(422):1–22

    Google Scholar 

  • Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417

    Article  Google Scholar 

  • Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853

    Article  CAS  Google Scholar 

  • Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269

    Article  CAS  Google Scholar 

  • Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733

    Article  CAS  Google Scholar 

  • Savage AM, Trapido-Rosenthal H, Douglas AE (2002) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Mar Ecol Prog Ser 244:27–37

    Article  Google Scholar 

  • Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Glob Change Biol 11:1–11

    Article  Google Scholar 

  • Stambler N, Dubinsky Z (2004) Stress effects on metabolism and photosynthesis of hermatypic corals. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 195–215

    Chapter  Google Scholar 

  • Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956

    Article  CAS  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13(4):178–182

    Article  CAS  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. PNAS 101:13531–13535

    Article  CAS  Google Scholar 

  • Tolleter D, Seneca FO, DeNofrio JC, Krediet CJ, Palumbi SR, Pringle JR, Grossman AR (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23:1782–1786

    Article  CAS  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59(5):1069–1080

    Article  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. PNAS 96:8007–8012

    Article  CAS  Google Scholar 

  • Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  CAS  Google Scholar 

  • Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23:369–376

    Article  Google Scholar 

  • Wicks LC, Hill R, Davy SK (2010) The influence of irradiance on tolerance to high and low temperature stress exhibited by Symbiodinium in the coral, Pocillopora damicornis, from the high-latitude reef of Lord Howe Island. Limnol Oceanogr 55(6):2476–2486

    Article  Google Scholar 

  • NIWA—National Institute of Water and Atmospheric Research Ltd. http://www.niwa.co.nz/

  • NOAA—National Oceanic and Atmospheric Administration. http://www.ncdc.noaa.gov/oa/climate/research/sst/sst.php

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to thank Scott Santos (Auburn University, Auburn, AL, USA), Mary Alice Coffroth (University of Buffalo, Buffalo, NY, USA), and Gisèle Muller-Parker (formerly Western Washington University, WA, USA) for the supply of some of our Symbiodinium cultures. We are also grateful to Jennifer Howe for her assistance in the laboratory. This work was supported by a Victoria University PhD Scholarship (to AW) and a Marsden Fund Grant from the Royal Society of New Zealand (VUW0902 to SKD and PLF).

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Wietheger, A., Fisher, P.L., Gould, K.S. et al. Sensitivity to oxidative stress is not a definite predictor of thermal sensitivity in symbiotic dinoflagellates. Mar Biol 162, 2067–2077 (2015). https://doi.org/10.1007/s00227-015-2736-3

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