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Under high light stress two Indo-Pacific coral species display differential photodamage and photorepair dynamics

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Abstract

The in hospite Symbiodinium symbiont of corals on shallow reefs relies on photoprotection and photorepair during periods of exposure to short-term high light and/or temperature stress. A coral’s susceptibility to bleaching is species specific and determined not only by Symbiodinium type, size and physiology, but also by coral host features. Here, photoprotective, photorepair, photochemical and non-photochemical efficiency parameters of Symbiodinium harboured in two morphologically different coral species were examined on Heron Island (23.4420°S, 151.9140°E) in July 2011. The two coral species were exposed to high light stress for 96 h, with or without inhibition of photosystem (PS) II repair by lincomycin. Symbiodinium harboured in Pocillopora damicornis showed an increase in xanthophyll de-epoxidation under high light exposure, whereas algal symbionts in Pavona decussata showed constant levels of xanthophyll de-epoxidation. High light-treated specimens of P. damicornis maintained steady PsbA protein (D1 protein) content throughout the experiment, but P. decussata showed a peak in PsbA protein content after 48 h of exposure. In hospite Symbiodinium in P. damicornis had greater content of PsbA protein fragments, suggesting higher accumulation of photodamaged products, compared to Symbiodinium in P. decussata, where both maintained steady PSII photochemical capacity over 96 h of exposure. Under inhibition of PSII repair, both species lost PsbA protein content and PSII photochemical capacity. Both species showed increased heat dissipation under inhibition of PSII repair, but differed in photoprotective strategies and photorepair activity. Our results suggest that, as well as any differences in the symbiont, characteristics of the coral host can alter important physiological responses in Symbiodinium.

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References

  • Anthony KRN, Hoegh-Guldberg O (2003) Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? Funct Ecol 17:246–259

    Article  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta (BBA)-Bioenerg 1143:113–134

    Article  CAS  Google Scholar 

  • Bachmann K, Ebbert V, Adams WI, Verhoeven A, Logan B, Demmig-Adams B (2004) Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery. Funct Plant Biol 31:803–813. doi:10.1071/FP04022

    Article  CAS  Google Scholar 

  • Brodersen KE, Lichtenberg M, Ralph PJ, Kühl M, Wangpraseurt D (2014) Radiative energy budget reveals high photosynthetic efficiency in symbiont-bearing corals. J R Soc Interface. doi:10.1098/rsif.2013.0997

    Google Scholar 

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

    Article  Google Scholar 

  • Brown BE, Downs C, Dunne RP, Gibb SW (2002) Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. J Exp Mar Biol Ecol 277:129–144

    Article  CAS  Google Scholar 

  • Brown CM, Campbell DA, Lawrence JE (2007) Resource dynamics during infections of Micromonas pusilla by virus MpV-Sp1. Environ Microbiol 9:2720–2727. doi:10.1111/j.1462-2920.2007.01384.x

    Article  CAS  Google Scholar 

  • Brown EM, MacKinnon Jd, Cockshutt AM, Villareal TA, Campbell DA (2008) Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Mar Biol. doi:10.1007/s00227-008-0933-z

    Google Scholar 

  • Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis. J Exp Biol 215:3467–3477

    Article  CAS  Google Scholar 

  • Burton GW (1990) Antioxidant properties of carotenoids. J Nutr 119:109–111

    Google Scholar 

  • Davies PS (1991) Effect of daylight variations on the energy budgets of shallow-water corals. Mar Biol 108:137–144

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the photoprotection of photosynthesis. Trends Biochem Sci 1:21–26

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88. doi:10.1007/s11120-012-9761-6

    Article  CAS  Google Scholar 

  • Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116

    Article  Google Scholar 

  • Downs CA et al (2013) Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching. PlosOne 8:e77173

    Article  CAS  Google Scholar 

  • Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34:418–430

    Article  Google Scholar 

  • Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620. doi:10.1007/s11120-008-9342-x

    Article  CAS  Google Scholar 

  • Edge R, Truscott GT (1999) Carotenoid radicals and the interaction of carotenoids with active oxygen species. In: Frank HA, Yound AJ, Britton G, Cogdell RJ (eds) The photochemistry of carotenoids, advances in photosynthesis, vol 8. Kluwer Academic Publishers, Dordrecht, pp 223–234

    Chapter  Google Scholar 

  • Edmunds PJ, Gates RD (2002) Normalizing physiological data for scleractinian corals. Coral Reefs 21:193–197

    Google Scholar 

  • Enriquez S, Mendez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032

    Article  Google Scholar 

  • Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR (1996) The lifetimes and energies of the first excited singlet states of diadinoxanthin and diatoxanthin: the role of these molecules in excess energy dissipation in algae. Biochim Biophys Acta 1277:243–252

    Article  CAS  Google Scholar 

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

    Article  CAS  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 

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

    Article  CAS  Google Scholar 

  • Grimsditch G, Mwaura J, Kilonzo J, Amiyo N, Obura D (2008) High zooxanthellae densities and turnover correlate with low bleaching tolerance in Kenyan corals. In: Obura DO, Tamelander J, Linden O (eds) Ten years after bleaching- facing the consequences of climate change in the Indian Ocean, vol 4. CORDIO Status Report 2008, vol 4. Coastal Oceans Research and Development in the Indian Ocean/Sida-SAREC, Mombasa, pp 235–236

  • Hawkins TD, Krueger T, Wilkinson SP, Fisher PL, Davy SK (2015) Antioxidant responses to heat and light stress differ with habitat in a common reef coral. Coral Reefs 34:1229–1241

    Article  Google Scholar 

  • Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81

    Article  CAS  Google Scholar 

  • Hennige SJ, McGinley MP, Grottoli AG, Warner ME (2011) Photoinhibition of Symbiodinium spp. within the reef corals Montastraea faveolata and Porites astreoides: implications for coral bleaching. Mar Biol 158:2515–2526. doi:10.1007/s00227-01101752-1

    Article  CAS  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, Ulstrup KE, Ralph PJ (2009) Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bull Mar Sci 85:223–244

    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 photoinactivation. Limnol Oceanogr 56:139–146

    Article  Google Scholar 

  • Hill R, Larkum AWD, Prášil O, Kramer DM, Kumar V, Ralph PJ (2012) Light-induced redistribution of antenna complexes in the symbionts of scleractinian corals correlates with sensitivity to coral bleaching. Coral Reefs 31:963–975. doi:10.1007/s00338-012-0941-z

    Article  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

    Article  Google Scholar 

  • Hoogenboom M, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154

    Article  Google Scholar 

  • Hoogenboom M, Campbell D, Beraud E, DeZeeuw K, Ferrier-Pagès C (2012) Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts. PlosOne 7:e30167. doi:10.1371/journal.pone.0030167

    Article  CAS  Google Scholar 

  • Jeans J, Campbell D, Hoogenboom MO (2013) Increased reliance upon photosystem II repair following acclimation to high-light by coral-dinoflagellate symbioses. Photosynth Res 118:219–229

    Article  CAS  Google Scholar 

  • Jimenez IM, Kuehl M, Larkum AWD, Ralph PJ (2008) Heat budget and thermal microenvironment of shallow-water corals: do massive corals get warmer than branching corals? Limnol Oceanogr 53:1548–1561

    Article  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99

    Article  CAS  Google Scholar 

  • Jupiter S, Roff G, Marion G, Henderson M, Schrameyer V, McCulloch M, Hoegh-Guldber O (2008) Linkages between coral assemblages and coral proxies of terrestrial exposure along a cross-shelf gradient on the southern Great Barrier Reef. Coral Reefs 27:887–903

    Article  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Klüter A, Crandall JB, Archer FI, Teece MA, Coffroth MA (2015) Taxonomic and environmental variation of metabolite profiles in marine dinoflagellates of the genus Symbiodinium. Metabolites 5:74–99. doi:10.3390/metabo5010074

    Article  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  Google Scholar 

  • Krämer WE, Caamaño-Ricken I, Richter C, Bischof K (2012) Dynamic regulation of photoprotection determines thermal tolerance of two phylotypes of Symbiodinium clade A at two photon fluence rates. Photochem Photobiol 88:398–413

    Article  Google Scholar 

  • Krämer WE, Schrameyer V, Hill R, Ralph PJ, Bischof K (2013) PSII activity and pigment dynamics of Symbiodinium in two Indo-Pacific corals exposed to short-term high-light stress. Marine Biol 160:563–577. doi:10.1007/s00227-012-2113-4

    Article  Google Scholar 

  • Krüger T et al (2015) Transcriptomic characterization of the enzymatic antioxidants FeSOD, MnSOD, APX and KatG in the dinoflagellate genus Symbiodinium. BMC Evolut Biol 15:1

    Article  Google Scholar 

  • Lavaud J, Six C, Campbell D (2015) Photosystem II repair in marine diatoms with contrasting photophysiologies. Photosynth Res PRES-D-15-00085R1

  • 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. Annu Rev Physiol 68:253–278. doi:10.1146/annurev.physiol.68.040104.110001

    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 Press, New York, pp 405–419

    Chapter  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, 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

    Article  Google Scholar 

  • Levy O, Dubinsky Z, Schneider K, Achituv Y, Zakai D, Gorbunov MY (2004) Diurnal hysteresis in coral photosynthesis. Mar Ecol Prog Ser 268:105–117

    Article  Google Scholar 

  • Li G, Brown CM, Jeans JA, Donaher N, McCarthy A, Campbell DA (2015) The nitrogen costs of photosynthesis in a diatom under current and future pCO2. New Phytol 205:533–543

    Article  CAS  Google Scholar 

  • MacIntyre HL, Kana T, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5:12–17

    Article  CAS  Google Scholar 

  • Marcelino LA et al (2013) Modulation of light-enhancement to symbiotic algae by light-scattering in corals and evolutionary trends in bleaching. PlosOne 8:e61492

    Article  CAS  Google Scholar 

  • Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M (1984) Regulation of protein metabolism coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81:1380–1384

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world: coral reefs. Elsevier, Amsterdam, pp 75–87

    Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330

    Article  CAS  Google Scholar 

  • Nixon PJ, Barker DH, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357–363

    Article  CAS  Google Scholar 

  • Pernice M, Dunn SR, Miard T, Dufour S, Dove S, Hoegh-Guldber O (2011) Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora. PlosOne 6:e16095

    Article  CAS  Google Scholar 

  • Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant sensitive phylotypes. Mar Ecol Prog Ser 406:57–70

    Article  CAS  Google Scholar 

  • Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104

    Article  CAS  Google Scholar 

  • Richardson MJ, Gardner WD, Chung SP, Walsh D (1993) Source of beam attenuation signal as a function of particle size The Oceanography Society Meeting Abstracts, Seattle, Washington, p 71

  • Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol 204:81–91

    Article  CAS  Google Scholar 

  • Roth MS, Latz MI, Goericke R, Deheyn DD (2010) Green fluorescent protein regulation in the coral Acropora yongei during photoacclimation. J Exp Biol 213:3644–3655

    Article  CAS  Google Scholar 

  • Salih A, Larkum AWD, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  CAS  Google Scholar 

  • Schreiber U (2004) Pulse-Amplitude-Modulation (PAM) Fluorometry and Saturation Pulse Method: An Overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19. Advances in Photosynthesis and Respiration. Springer, Govindje, pp 279-319

  • Schreiber U, Hormann H, Asada K, Neubauer C (1995) O2-dependent electron flow in intact spinach chloroplasts: properties and possible regulation of the Mehler-ascorbate-Peroxidase cycle. In: Mathis P (ed) Photosynthesis: from Light to Biosphere, vol II. Kluwer Academic Publishers, Dordrecht, pp 813–818

    Google Scholar 

  • Shipton CA, Barber J (1991) Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: evidence for an autoproteolytic process triggered by the oxidizing of the photosystem. Proc Natl Acad Sci USA 88:6691–6695

    Article  CAS  Google Scholar 

  • Six C, Finkel ZV, Irwin AJ, Campbell DA (2007) Light variability illuminates niche-partitioning among marine picocyanobacteria. Plos One 2:e1341. doi:10.1371/journal/pone.0001341

    Article  Google Scholar 

  • Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Biol 153:66–74

    Google Scholar 

  • Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME, Ralph PJ (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381

    Article  Google Scholar 

  • Swain TD et al (2016) Skeletal light-scattering accelerates bleaching response in reef-building corals. BMC Ecol. doi:10.1186/s12898-016-0061-4

    Google Scholar 

  • Szabó M et al (2014) Effective light absorption and absolute electron transport rates in the coral Pocillopora damicornis. Plant Physiol Biochem 83:159–167

    Article  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 45:231–235

    Google Scholar 

  • Takahashi S, Whitney SM, Badger MR (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci 106:3237–3242

    Article  CAS  Google Scholar 

  • Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142:6–16

    Article  CAS  Google Scholar 

  • Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta- Bioenerg 1871:209–217

    Article  Google Scholar 

  • Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:1360–1385

    Article  Google Scholar 

  • Wang JT, Douglas AE (1997) Nutrients, signals, and photosynthate release by symbiotic algae: the impact of taurine on the dinoflagellate alga Symbiodinium from the sea anemone Aiptasia pulchella. Plant Physiol 114:631–636

    Article  CAS  Google Scholar 

  • Wang JT, Douglas AE (1999) Essential amino acid synthesis and nitrogen recycling in an alga-invertebrate symbiosis. Mar Biol 135:219–222

    Article  CAS  Google Scholar 

  • Wangpraseurt D, Larkum AWD, Ralph PJ, Kühl M (2012) Light gradients and optical microniches in coral tissues. Front Microbiol 3:316. doi:10.3389/fmicb.2012.00316

    Article  Google Scholar 

  • Wangpraseurt D, Larkum AWD, Franklin J, Szabó M, Ralph PJ, Kühl M (2014) Lateral light transfer ensures efficient resource distribution in symbiont-bearing corals. J Exp Biol 217:489–498

    Article  Google Scholar 

  • Warner ME, Berry-Lowe S (2006) Differential xanthophyll cycling and photochemical activity in symbiotic dinoflagellates in multiple locations of three species of Caribbean coral. J Exp Mar Biol Ecol 339:86–95

    Article  CAS  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 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 

  • Whitehead LF, Douglas AE (2003) Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. J Exp Biol 206:3149–3157

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the staff at Heron Island research station and Malin Gustaffson for support during fieldwork, and the University of Technology, Sydney, for financial support for travel to the field site. The Australian Coral Reef Society supported the fieldwork through the Terry Walker prize awarded to VS. NSERC of Canada supported a graduate scholarship to JJ and the costs of the protein analyses. We thank Australian Research Council for PhD project of VS and infrastructure support.

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Schrameyer, V., Krämer, W., Hill, R. et al. Under high light stress two Indo-Pacific coral species display differential photodamage and photorepair dynamics. Mar Biol 163, 168 (2016). https://doi.org/10.1007/s00227-016-2940-9

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