Skip to main content

Antioxidant responses to heat and light stress differ with habitat in a common reef coral

Abstract

Coral bleaching—the stress-induced collapse of the coral–Symbiodinium symbiosis—is a significant driver of worldwide coral reef degradation. Yet, not all corals are equally susceptible to bleaching, and we lack a clear understanding of the mechanisms underpinning their differential susceptibilities. Here, we focus on cellular redox regulation as a potential determinant of bleaching susceptibility in the reef coral Stylophora pistillata. Using slow heating (1 °C d−1) and altered irradiance, we induced bleaching in S. pistillata colonies sampled from two depths [5–8 m (shallow) and 15–18 m (deep)]. There was significant depth-dependent variability in the timing and extent of bleaching (loss of symbiont cells), as well as in host enzymatic antioxidant activity [specifically, superoxide dismutase and catalase (CAT)]. However, among the coral fragments that bleached, most did so without displaying any evidence of a host enzymatic antioxidant response. For example, both deep and shallow corals suffered significant symbiont loss at elevated temperature, but only deep colonies exposed to high temperature and high light displayed any up-regulation of host antioxidant enzyme activity (CAT). Surprisingly, this preceded the equivalent antioxidant responses of the symbiont, which raises questions about the source(s) of hydrogen peroxide in the symbiosis. Overall, changes in enzymatic antioxidant activity in the symbionts were driven primarily by irradiance rather than temperature, and responses were similar across depth groups. Taken together, our results suggest that in the absence of light stress, heating of 1 °C d−1 to 4 °C above ambient is not sufficient to induce a substantial oxidative challenge in S. pistillata. We provide some of the first evidence that regulation of coral enzymatic antioxidants can vary significantly depending on habitat, and, in terms of determining bleaching susceptibility, our results suggest a significant role for the host’s differential regulation of cellular redox status.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Armoza-Zvuloni R, Shaked Y (2014) Release of hydrogen peroxide and antioxidants by the coral Stylophora pistillata to its external milieu. Biogeosci Discuss 11:33–59

    Article  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 228–287

    Google Scholar 

  • Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2008) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20

    Article  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beers R, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  PubMed  Google Scholar 

  • Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proc R Soc Lond B Biol Sci 279:1100–1107

    Article  CAS  Google Scholar 

  • Berkelmans R, van Oppen MJH (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 Lond B Biol Sci 273:2305–2312

    Article  Google Scholar 

  • Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871

    Article  PubMed Central  PubMed  Google Scholar 

  • Bowler C, Van Camp W, Van Montagu M, Inze D (1994) Superoxide dismutase in plants. CRC Crit Rev Plant Sci 13:199–218

    Article  CAS  Google Scholar 

  • Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326

    Article  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543

    Article  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: are the batteries of the reef going to run out? PLoS One 7:e39024

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dykens JA, Shick JM (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580

    Article  CAS  Google Scholar 

  • Dykens JA, Shick JM (1984) Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects, and seasonal photoacclimatization. Biol Bull 167:683–697

    Article  CAS  Google Scholar 

  • Ernst O, Zor T (2010) Linearization of the Bradford protein assay. J Vis Exp 38:e1918

    Google Scholar 

  • Fabricius KE (2006) Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: implications for coral bleaching? Limnol Oceanogr 51:30–37

    Article  Google Scholar 

  • Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses. Mol Ecol Res 12:369–373

    Article  Google Scholar 

  • Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Nino-Southern oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

  • Goreau TF (1990) Coral bleaching in Jamaica. Nature 343:417

    Article  Google Scholar 

  • Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20:3823–3833

    Article  PubMed  Google Scholar 

  • Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7:e33353

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hawkins TD, Davy SK (2013) Nitric oxide and coral bleaching: is peroxynitrite generation required for symbiosis collapse? J Exp Biol 216:3185–3188

    Article  CAS  PubMed  Google Scholar 

  • Hawkins TD, Krueger TK, 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 

  • Jones RJ (2008) Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Mar Biol 154:65–80

    Article  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 

  • Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

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

    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. Annu Rev Physiol 68:253–278

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky TJ, Stamler JS (eds) Coral reefs: an ecosystem in transition. Springer, Berlin, 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 

  • Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377

    Article  Google Scholar 

  • Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232

    Article  Google Scholar 

  • Levy O, Achituv Y, Yacobi YZ, Stambler N, Dubinsky Z (2006) The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus. J Exp Mar Biol Ecol 328:35–46

    Article  CAS  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Muscatine L, Hand C (1958) Direct evidence for the transfer of materials from symbiotic algae to the tissues of a coelenterate. Proc Natl Acad Sci U S A 44:1259–1263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945

    Article  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:444–456

    Article  CAS  Google Scholar 

  • Paxton CW, Davy SK, Weis VM (2013) Stress and death of host cells play a role in cnidarian bleaching. J Exp Biol 216:2813–2820

    Article  PubMed  Google Scholar 

  • Pontasch S, Hill R, Deschaseaux E, Fisher P, Davy S, 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 

  • Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc Lond B Biol Sci 279:4352–4361

    Article  Google Scholar 

  • Radi R, Peluffo G, Alvarez MN, Naviliat M, Cayota A (2001) Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med 30:463–488

    Article  CAS  PubMed  Google Scholar 

  • Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci U S A 105:13674–13678

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Richier S, Furla P, Plantivaux A, Merle PL, Allemand D (2005) Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208:277–285

    Article  PubMed  Google Scholar 

  • Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273:4186–4198

    Article  CAS  PubMed  Google Scholar 

  • Richier S, Cottalorda J-M, Guillarme MMM, Fernandez C, Allemand D, Furla P (2008) Depth-dependent response to light of the reef building coral, Pocillopora verrucosa: implication of oxidative stress. J Exp Mar Biol Ecol 357:48–56

    Article  CAS  Google Scholar 

  • Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saragosti E, Tchernov D, Katsir A, Shaked Y (2010) Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. PLoS One 5:e12508

    Article  PubMed Central  PubMed  Google Scholar 

  • Shick JM, Lesser MP, Dunlap WC, Stochaj WR, Chalker BE, Won JW (1995) Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar Biol 122:41–51

    Article  CAS  Google Scholar 

  • Silverstein RN, Cunning R, Baker AC (2014) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Bio. 21:236–249

    Article  Google Scholar 

  • Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96

    Article  CAS  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 

  • Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, Rosenfeld H, Falkowski PG (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci U S A 108:9905–9909

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tolleter D, Seneca F, DeNofrio J, Krediet C, Palumbi S, Pringle J, Grossman A (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23:1782–1786

    Article  CAS  PubMed  Google Scholar 

  • Traylor-Knowles N, Palumbi SR (2014) Translational environmental biology: cell biology informing conservation. Trends Cell Biol 24:265–267

    Article  PubMed  Google Scholar 

  • Veal CJ, Holmes G, Nunes M, Hoegh-Guldberg O, Osborne J (2010) A comparative study of methods for surface area and three dimensional shape measurement of coral skeletons. Limnol Oceanogr Methods 8:241–253

    Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–8012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Winterbourn CC (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4:278–286

    Article  CAS  PubMed  Google Scholar 

  • Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B Biochem Mol Biol 139:721–730

    Article  CAS  PubMed  Google Scholar 

  • Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank the staff at Heron Island Research Station, University of Queensland, for their assistance with sampling and equipment maintenance, and Dr Olga Pantos for providing storage space for samples during transit. This work was carried out as part of a PhD project supported by a Commonwealth Scholarship awarded to TH, a Marsden Fund award (#VUW0902) to SKD and PF, a Marsden-funded PhD scholarship to TK, and a Victoria University of Wellington Vice Chancellor’s Strategic Research PhD Scholarship to SPW. Finally, we thank Dr Mark Warner, members of the Davy Lab and four anonymous reviewers for their constructive feedback.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simon K. Davy.

Additional information

Communicated by Biology Editor Dr. Line K. Bay

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hawkins, T.D., Krueger, T., Wilkinson, S.P. et al. Antioxidant responses to heat and light stress differ with habitat in a common reef coral. Coral Reefs 34, 1229–1241 (2015). https://doi.org/10.1007/s00338-015-1345-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-015-1345-4

Keywords

  • Coral bleaching
  • Cnidarian–dinoflagellate symbiosis
  • Symbiodinium
  • Stylophora pistillata
  • Oxidative stress
  • Climate change