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Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress

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Abstract

Elevated seawater temperatures have long been accepted as the principal stressor causing the loss of symbiotic algae in corals and other invertebrates with algal symbionts (i.e., “bleaching”). A secondary factor associated with coral bleaching is solar irradiance, both its visible (PAR: 400–700 nm) and ultraviolet (UVR: 290–400 nm) portions of the spectrum. Here we examined the synergistic role of solar radiation on thermally induced stress and subsequent bleaching in a common Caribbean coral, Montastraea faveolata. Active fluorescent measurements show that steady-state quantum yields of photosystem II (PSII) fluorescence in the zooxanthellae are markedly depressed when exposed to high solar radiation and elevated temperatures, and the concentration of D1 protein is significantly lower in high light when compared to low light treatments under the same thermal stress. Both photosynthetic pigments and mycosporine-like amino acids (MAAs) are also depressed after experimental exposure to high solar radiation and thermal stress. Host DNA damage is exacerbated under high light conditions and is correlated with the expression of the cell cycle gene p 53, a cellular gatekeeper that modulates the fate of damaged cells between DNA repair processes and apoptotic pathways. These markers of cellular stress in the host and zooxanthellae have in common their response to the enhanced production of reactive oxygen species during exposure to high irradiances of solar radiation and elevated temperatures. Taking these results and previously published data into consideration, we conclude that thermal stress during exposure to high irradiances of solar radiation, or irradiances higher than the current photoacclimatization state, causes damage to both photochemistry and carbon fixation at the same time in zooxanthellae, while DNA damage, apoptosis, or necrosis are occurring in the host tissues of symbiotic cnidarians.

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Abbreviations

σPSII :

Functional absorption cross-section for PSII

Fo, Fm :

Minimum and maximum yields of chlorophyll a fluorescence measured after dark acclimation (relative units)

Fv :

Variable fluorescence after dark acclimation (=Fm−Fo), dimensionless

Fv/Fm :

Maximum quantum yield of photochemistry in PSII measured after dark acclimation, dimensionless

F′, Fm′:

Steady-state and maximum yields of chlorophyll a fluorescence measured under ambient light (relative units)

ΔF/Fm′:

Quantum yield of photochemistry in PSII measured at steady state under ambient light

References

  • Anderson S, Zepp R, Machula J, Santavy D, Hansen L, Mueller D (2001) Indicators of UV exposure in corals and their relevance to global climate change and coral bleaching. Human Ecol Risk Asses 7:1271–1282

    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

  • Bhagooli R, Hidaka M (2004) Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses. Comp Biochem Physiol 137:547–555

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophylls concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM (2000) A molecular biomarker system for assessing the health of coral ( Montastraea faveolata) during heat stress. Mar Biotechnol 2:533–544

    Article  CAS  PubMed  Google Scholar 

  • Dunlap WC, Chalker BE (1986) Identification and quantitation of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:153–159

    Google Scholar 

  • Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol 112B:106–114

    Google Scholar 

  • Dunn SR, Bythell JC, Le Tessier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53

    Article  Google Scholar 

  • Dunne RP, Brown BE (2001) The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs 20:201–210

    Google Scholar 

  • Dustan P (1982) Depth-dependent photoadaptation by zooxanthellae of the reef coral Montastrea annularis. Mar Biol 68:253–264

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Dykens JA, Shick JM, Benoit C, Buettner GR, Winston GW (1992) Oxygen radical production in the sea anemone Anthopleura elegantissima and its symbiotic algae. J Exp Biol 168:219–241

    CAS  Google Scholar 

  • Evans G, Littlewood T (1998) A matter of life and cell death. Science 281:1317–1322

    Article  PubMed  Google Scholar 

  • Falkowski PG, Kolber Z (1993) Estimate of phytoplankton photosynthesis by active fluorescence. ICES Mar Sci Symp 197:92–103

    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 

  • Fitt WK, Spero HJ, Halas J, White MW, Porter JW (1993) Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “bleaching event”. Coral Reefs 12:57–64

    Google Scholar 

  • Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11

    CAS  PubMed  Google Scholar 

  • Fridovich I (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201:1203–1209

    CAS  PubMed  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

    Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838

    Article  Google Scholar 

  • Glynn PW (1991) Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol Evol 6:175–179

    Article  Google Scholar 

  • Glynn PW, D’Croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191

    Google Scholar 

  • Glynn PW, Imai R, Sakai K, Nakano Y, Yamazato K (1992) Experimental responses of Okinawan (Ryukyu Islands, Japan) reef corals to high sea temperature and UV radiation. In: Richmond R (ed) Proceedings of the Seventh Coral Reef Symposium, Guam. University of Guam, pp 27–37

  • Gorbunov M, Falkowski PG, Kolber Z (2000) Measurement of photosynthetic parameters in benthic organisms in situ using a SCUBA-based fast repetition rate fluorometer. Limnol Oceanogr 45:242–245

    Google Scholar 

  • Gorbunov M, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85

    CAS  Google Scholar 

  • Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK, and Edelman M (1989) Separate photosensitizers mediate degradation of the 32 kDa photosystem II reaction center protein in the visible and UV spectral regions. Proc Natl Acad Sci 86:6617–6620

    CAS  PubMed  Google Scholar 

  • Hale AJ, Smith CA, Sutherland LC, Stoneman VE, Longthorne VL, Culhane AC, Williams GT (1996) Apoptosis: molecular regulation of cell death. Eur J Biochem 236:1–26

    CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford Science Publications, London, 936 pp

  • Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86

    Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol 129:279–303

    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 89:10302–10305

    CAS  PubMed  Google Scholar 

  • Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309

    CAS  PubMed  Google Scholar 

  • Inglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175

    Google Scholar 

  • Inglesias-Prieto R, Trench, RK (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar Ecol Prog Ser 130:23–33

    Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c , and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    CAS  Google Scholar 

  • Jokiel PL, Coles SL (1990) Responses of Hawaiian and other Indo-Pacific reef corals to elevated temperatures. Coral Reefs 8:155–162

    Google Scholar 

  • Jokiel PL, Lesser MP, Ondrusek ME (1997) UV-absorbing compounds in the coral Pocillopora damicornis: interactive effects of UV radiation, photosynthetically active radiation, and water flow. Limnol Oceanogr 42:1468–1473

    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 

  • Kelly ML, Winge P, Heaney JD, Stephens RE, Farell JH, Van Beneden RJ, Reinisch CL, Lesser MP, Walker CW (2001) Expression of homologues for p53 and p73 in the softshell clam ( Mya arenaria), a naturally-occurring model for human cancer. Oncogene 20:748–758

    Article  PubMed  Google Scholar 

  • Kim CS, Lim WA, Cho YC (2001) Mycosprine-like amino acids as the UV sunscreen with oxygen radical scavenging activity. Bull Natl Fish Res Dev Inst Korea 60:65–71

    Google Scholar 

  • Kirk JTO (1994) Optics of UV-B radiation in natural waters. Arch Hydrobiol Ergebnisse der Limnologie 43:1–16

    Google Scholar 

  • Kolber Z, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochem Biophys Acta 1367:88–106

    Article  CAS  PubMed  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • Lasker HR, Peters EC, Coffroth MA (1984) Bleaching of reef coelenterates in the San Blas Islands, Panama. Coral Reefs 3:183–190

    Google Scholar 

  • Lesser MP (1996) Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnol Oceanogr 41:271–283

    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 (2000) Depth-dependent effects of ultraviolet radiation on photosynthesis in the Caribbean coral, Montastraea faveolata. Mar Ecol Prog Ser 192:137–151

    Google Scholar 

  • Lesser MP, Gorbunov MY (2001) Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Mar Ecol Prog Ser 212:69–77

    CAS  Google Scholar 

  • Lesser MP, Lewis S (1996) Action Spectra for the Inhibition of Photosynthesis by Ultraviolet Radiation in the Hermatypic Coral, Pocillopora damicornis. Mar Ecol Prog Ser134:171–177

    Google Scholar 

  • Lesser MP, Shick JM (1989) Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity. Mar Biol 102:243–255

    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

    Google Scholar 

  • Lesser MP, Turtle SL, Farrell JH, Walker CW (2001) Exposure to ultraviolet radiation (290–400 nm) causes oxidative stress, DNA damage, and expression of p 53/73 in laboratory experiments on embryos of the spotted salamander, Ambystoma maculatum. Physiol Biochem Zool 74:733–741

    Article  CAS  PubMed  Google Scholar 

  • Lupínková L, Komenda J (2004) Oxidative modifications of the photosystem II D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochem Photobiol 79:152–162

    Article  PubMed  Google Scholar 

  • Macpherson AN, Telfer A, Barber J, Truscott TG (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centers. Biochem Biophys Acta 1143:301–309

    Article  CAS  Google Scholar 

  • Marsh JA (1970) Primary productivity of reef-building calcareous algae. Ecology 51:255–263

    Google Scholar 

  • Mori T, Nakane M, Hattori T, Matsunaga T, Ihara M, Nikaido O (1991) Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimers or (6–4) photoproduct from the same mouse immunized with ultraviolet radiated DNA. Photochem Photobiol 54:225–232

    CAS  PubMed  Google Scholar 

  • Mumby PJ, Chisholm JRM, Edwards AJ, Andrefouet S, Jaubert J (2001) Cloudy weather may have saved Society Island reef corals during 1998 ENSO event. Mar Ecol Prog Ser 222:209–216

    Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. I. 13C of zooxanthellae and animal tissue vs. depth. Mar Biol 100:185–193

    Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO 20:5587–5594

    Article  CAS  Google Scholar 

  • Polyak K, Xla Y, Zweler JL, Kinzler KW, Vogelstein B (1997) A model for p 53 induced apoptosis. Nature 389:300–305

    Article  CAS  PubMed  Google Scholar 

  • Renzing J, Hansen S, Lane DP (1996) Oxidative stress is involved in the UV activation of p 53. J Cell Sci 109:1105–1112

    CAS  PubMed  Google Scholar 

  • Richter M, Rühle W, Wild A (1990) Studies on the mechanism of photosystem II photoinhibition II. The involvement of toxic oxygen species. Photosyn Res 24:237–243

    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  PubMed  Google Scholar 

  • Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8:539–553

    Article  CAS  PubMed  Google Scholar 

  • Shick JM, Dunlap WC, Chalker BE, Banaszak AT, Rosenzweig TK (1992) Survey of ultraviolet radiation-absorbing mycosporine-like amino acids in organs of coral reef holothuroids. Mar Ecol Prog Ser 90:139–148

    CAS  Google Scholar 

  • Shick JM, Lesser MP, Jokiel PK (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biol 2:527–545

    Google Scholar 

  • Smith NP (2001) Weather and hydrographic conditions associated with coral bleaching: Lee Stocking Island, Bahamas. Coral Reefs 20:415–422

    Article  Google Scholar 

  • Strömgren T (1987) The effect of light on the growth rate of intertidal Acropora pulchra (Brook) from Phuket, Thailand, lat. 8° N. Coral Reefs 6:43–47

    Google Scholar 

  • Sukenick A, Bennett J, Falkowski PG (1987) Light-saturates photosynthesis-limitation by electron transport or carbon fixation? Biochim Biophys Acta 891:205–215

    Google Scholar 

  • Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef building corals. Plant Cell Physiol 45:251–255

    Article  CAS  PubMed  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1996) The effect 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

    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 USA 96:8007–8012

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was funded in part by a grant from the NOAA National Undersea Research Program through the Caribbean Marine Research Center at Lee Stocking Island, Bahamas. The views expressed herein are those of the author and do not necessarily reflect the views of NOAA or any of its sub-agencies. Support was also provided by the Office of Naval Research-Environmental Optics Program under Grant # 97PR00617–00 to MPL. I would like to thank the staff of Caribbean Marine Research Center at Lee Stocking Island for providing the field temperature data and excellent support during this work. I would like to thank Dr. Kozi Asada for the Cu/Zn SOD antibody and Dr. Toshio Mori for the CPD antibody. I would also like to thank Dr. Max Gorbunov for making the fast repetition rate fluorometer available for this work, and Drs. Chris Neefus and Geoff Trussell for assistance on the statistical analysis of the fluorescence data. The experiments conducted for this study comply with the current laws of the Bahamas and the United States of America.

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Correspondence to Michael P. Lesser.

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Communicated by R.C. Carpenter

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Lesser, M.P., Farrell, J.H. Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23, 367–377 (2004). https://doi.org/10.1007/s00338-004-0392-z

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