Abstract
Ocean acidification is thought to exert a major impact on calcifying organisms, including corals. While previous studies have reported changes in the physiological response of corals to environmental change, none have described changes in expression of the ubiquitous host pigments—fluorescent proteins (FPs)—to ocean acidification. The function of FPs in corals is controversial, with the most common consideration being that these primarily regulate the light environment in the coral tissue and protect the host from harmful UV radiation. Here, we provide for the first time experimental evidence that increased fluorescence of colonies of the coral Stylophora pistillata is independent of stress and can be regulated by a non-stressful decrease in pH. Stylophora pistillata is the most abundant and among the most resilient coral species in the northern Gulf of Eilat/Aqaba (GoE/A). Fragmented “sub-colonies” (n = 72) incubated for 33 days under three pH treatments (ambient, 7.9, and 7.6), under ambient light, and running seawater showed no stress or adverse physiological performance, but did display significantly higher fluorescence, with lower pH. Neither the average number of planulae shed from the experimental sub-colonies nor planulae green fluorescent protein (GFP) expression changed significantly among pH treatments. Sub-colonies incubated under the lower-than-ambient pH conditions showed an increase in both total protein and GFP expression. Since extensive protein synthesis requires a high level of transcription, we suggest that GFP constitutes a UV protection mechanism against potential RNA as well as against DNA damage caused by UV exposure. Manipulating the regulation of FPs in adult corals and planulae, under controlled and combined effects of pH, light, and temperature, is crucial if we are to obtain a better understanding of the role played by this group of proteins in cnidarians.








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References
Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs 27(3):485–490
Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci U S A 107(47):20400–20404
Bellworthy, J. & Fine, M. Coral Reefs (2017) https://doi.org/10.1007/s00338-017-1598-1
Ben-Zvi O, Eyal G, Loya Y (2014) Light-dependent fluorescence in the coral Galaxea fascicularis. Hydrobiologia 759(1):15–26
Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral reefs 23(1):74–83
Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta 1760:1690–1695
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254
Casati P, Walbot V (2004) Crosslinking of ribosomal proteins to RNA in maize ribosomes by UV-B and its effects on translation. Plant physiology 136(2):3319–3332
D’Angelo C, Smith EG, Oswald F, Burt J, Tchernov D, Wiedenmann J (2012) Locally accelerated growth is part of the innate immune response and repair mechanisms in reef-building corals as detected by green fluorescent protein (GFP)-like pigments. Coral Reefs 31(4):1045–1056
D’Angelo C, Denzel A, Vogt A, Matz MV, Oswald F, Salih A, Nienhaus GU, Wiedenmann J (2008) Blue light regulation of host pigment in reef-building corals. Mar Ecol Prog Ser 364:97–106
Date and Time (2017) https://www.timeanddate.com
De Gruijl FR, Van Kranen HJ, Mullenders LHF (2001) UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J Photochem Photobiol B 63(1–3):19–27
Dove SG, Lovell C, Fine M, Deckenback J, Hoegh-Guldber O, Iglesias-Prieto R, Anthony K (2008) Host pigments: potential facilitators of photosynthesis in coral symbioses. Plant Cell Environ 31(11):1523–1533
Eyal G, Wiedenmann J, Grinblat M, D’Angelo C, Kramarsky-Winter E, Treibitz T, Ben-Zvi O, Shaked Y, Smith TB, Harii S, Denis V, Noyes T, Tamir R, Loya Y (2015) Spectral diversity and regulation of coral fluorescence in a mesophotic reef habitat in the red sea PLoS One 10(6)
Gabay Y, Benayahu Y, Fine M (2013) Does elevated pCO2 affect reef octocorals? Ecol Evol 3(3):465–473
Gilmore AM, Larkum AW, Salih A, Itoh S, Shibata Y, Bena C, Yamasaki H, Papina M, Van Woesik R (2003) Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem Photobiol 77(5):515–523
Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2(6):495–509
Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral Reef Ecosystems under Climate Change and Ocean Acidification. Front Mar Sci 4:158
Horwitz R, Fine M (2014) High CO2 detrimentally affects tissue regeneration of Red Sea corals. Coral Reefs 33(3):819–829
Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalisation; strategies and considerations. Genes Immun 6(4):279
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 U S A 89(21):10302–10305
Iguchi A, Ozaki S, Nakamura T, Inoue M, Tanaka Y, Suzuki A, Kawahata H, Sakai K (2012) Effects of acidified seawater on coral calcification and symbiotic algae on the massive coral Porites australiensis. Mar Environ Res 73:32–36
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194
Krueger T, Horwitz N, Bodin J, Giovani ME, Escrig S, Meibom A, Fine M (2017) Common reef-building coral in the Northern Red Sea resistant to elevated temperature and acidification. R Soc Open Sci 4(5):170038
Kvitt H, Rosenfeld H, Zandbank K, Tchernov D (2011) Regulation of apoptotic pathways by Stylophora pistillata (anthozoa, pocilloporidae) to survive thermal stress and bleaching. PLoS One 6(12)
Krief S, Hendy EJ, Fine M, Yam R, Meibom A, Foster GL, Shemesh A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim Cosmochim Acta 74(17):4988–5001
Lecointe A, Domart-coulon I, Paris A, Meibom A, Domart-coulon I (2016) Cell proliferation and migration during early development of a symbiotic scleractinian coral. Proc R Soc Lond B Biol Sci. 283(1831)
Leutenegger A, D’Angelo C, Matz MV, Denzel A, Oswald F, Salih A, Nienhaus GU, Wiedenmann J (2007) It’s cheap to be colorful: Anthozoans show a slow turnover of GFP-like proteins. FEBS J 274(10):2496–2505
Loya Y (1976) The Red Sea coral Stylophora pistillata is an r strategist. Nature 259:478–480
Loya Y (1972) Community structure and species diversity of hermatypic corals at Eilat. Red Sea. J Mar Biol 13(2):100–123
Maier T, Güell M, Serrano L (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett 583(24):3966–3973
Marubini F, Ferrier-Pages C, Furla P, Allemand D (2008) Coral calcification responds to seawater acidification: A working hypothesis towards a physiological mechanism. Coral Reefs 27(3):491–499
Matz MV, Marshall NJ, Vorobyev M (2006) Are corals colorful? Photochem Photobiol 82(2):345–350
Monastersky R (2013) Global carbon dioxide levels near worrisome milestone. Nature 497(7447):13
Nakamura T, Van Woesik R, Yamasaki H (2005) Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Mar Ecol Prog Ser 301:109–118
NMP (2006) National monitoring Program for the Gulf of Aqaba http://www.meteo-tech.co.il/eilat-yam/eilat_en.asp
Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS One 4(10)
Pachauri RK, Allen MR, Barros VR, Broome J, Cramer W, Christ R, Church JA, Clarke L, Dahe Q, Dasgupta P, Dubash NK (2014) Climate change 2014: synthesis Report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change (p. 151). IPCC
Permata WD, Kinzie Iii RA, Hidaka M (2000) Histological studies on the origin of planulae of the coral Pocillopora damicornis. Mar Ecol Prog Ser 200:191–200
Ravanat JL, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B 63(1–3):88–102
Reynaud S, Leclercq N, Romaine-Liuod S, Ferrier-Pages C, Jaubert J, Gattuso JP (2003) Interacting effects of CO 2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9:1660–1668
Rinkevich B, Loya Y (1979a) The reproduction of the Red Sea coral Stylophora pistillata. I. Gonads and planulae. Mar Ecol Prog Ser 1:133–144
Rinkevich B, Loya Y (1979b) The reproduction of the Red Sea coral Stylophora pistillata. II. Synchronization in breeding and seasonality of planulae shedding. Mar Ecol Prog Ser 1:145–152
Roth MS, Deheyn DD (2013) Effects of cold stress and heat stress on coral fluorescence in reef-building corals. Scientific Reports 3:1421
Roth MS, Fan TY, Deheyn DD (2013) Life History Changes in Coral Fluorescence and the Effects of Light Intensity on Larval Physiology and Settlement in Seriatopora hystrix PLoS One 8(3)
Roth MS, Latz MI, Goericke R, Deheyn DD (2010) Green fluorescent protein regulation in the coral Acropora yongei during photoacclimation. J Exp Biol 213(21):3644–3655
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Salih A, Larkum A, Cox G (2001) Photoprotection from photoinhibition of symbiotic algae in corals by fluorescent pigments. Science Access 3(1):1–4
Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408(6814):850–853
Smith-Keune C, Dove S (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Mar Biotechnol 10(2):166–180
Smith EG, D’Angelo C, Salih A, Wiedenmann J (2013) Screening by coral green fluorescent protein (GFP)-like chromoproteins supports a role in photoprotection of zooxanthellae. Coral Reefs 32(2):463–474
Sparks JS, Schelly RC, Smith WL, Davis MP, Tchernov D, Pieribone VA, Gruber DF (2014) The covert world of fish biofluorescence: A phylogenetically widespread and phenotypically variable phenomenon. PLoS One 9(1)
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 Mar Bio Ecol 153(1):63–74
Wheeler B (2010) lmPerm: Permutation tests for linear models. R package version 1.1-2. https://CRAN.R-project.org/package=lmPerm
Wurtmann EJ, Wolin SL (2009) RNA under attack: cellular handling of RNA damage. Crit Rev Biochem Mol Biol 44(1):34–49
Acknowledgements
We thank the Interuniversity Institute for Marine Sciences at Eilat (IUI for the logistical support. We are indebted to Tom Shlesinger, Hanna Rapuano, Dror Komet, Yoav Lindemann, and Jessica Bellworthy for help in field work and aquaria maintenance and Dr. Roi Holtzman and Itai Granot for statistical advice. Special thanks are due to Naomi Paz for copy editing the manuscript. This study was partially supported by the Israel Science Foundation (ISF) No. 341/12 and the U.S. Middle East Regional Cooperation (MERC) Program Agency for International Development (MERC/USAID) No. M32-037 to Y.L.
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Grinblat, M., Fine, M., Tikochinski, Y. et al. Stylophora pistillata in the Red Sea demonstrate higher GFP fluorescence under ocean acidification conditions. Coral Reefs 37, 309–320 (2018). https://doi.org/10.1007/s00338-018-1659-0
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DOI: https://doi.org/10.1007/s00338-018-1659-0