Why Don t Corals Get Sunburned?

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1 Why Don t Corals Get Sunburned? Author: J. Malcolm SHICK Professor Emeritus of Zoology and Oceanography, School of Marine Sciences, University of Maine, Orono, Maine, U.S.A. First-time visitors to a tropical coral reef are astonished by the diversity and abundance of organisms living there, especially by the shapes and colors of corals looking like rocks and stony trees but which actually are colonial animals that build the reef. Tourists learn quickly and painfully about the brightness of the tropical sun and the clarity of the water, and how easily one becomes sunburned if not protected. Yet as the physiologist Paul Portier (who had sailed often with Prince Albert I of Monaco on his oceanographic expeditions) saw on his visit to the Great Barrier Reef, corals thrive and flower under tropical solar irradiation. Indeed, sunlight and clear seawater are necessary for the development of healthy coral reefs. Photo 1: Corals living in shallow waters on the Great Barrier Reef are exposed to some of the highest levels of potentially damaging solar ultraviolet radiation on Earth. Photo: J.M. Shick. The water is clear because it is low in nutrients and therefore in phytoplankton the tiny floating algae that are the basis of many marine food webs. Instead, millions of single-celled algae, commonly called zooxanthellae, live within the gastrodermal cells lining the digestive cavity of corals, forming a quintessential solar-powered symbiosis. The algae capture sunlight in photosynthesis and provide to the host animal most of the organic material that they produce. In return the host recycles its wastes such as

2 carbon dioxide (from respiration) and ammonia (from protein metabolism) as fertilizer for the algae. But for the algae to photosynthesize, their animal hosts must expose themselves to bright tropical sunlight, including its component of ultraviolet radiation (UVR). Corals living in shallow waters on the Great Barrier Reef may be exposed daily to 30 times the minimum dose of solar UVR that causes erythema (skin reddening) in humans. In clear water low in dissolved organic compounds that would absorb solar UVR, these wavelengths actually penetrate beneath the surface. So, why don t tropical corals get sunburned? As humans are encouraged to do, corals use sunscreens that absorb the potentially damaging UV wavelengths of sunlight before these can harm their tissues. Solar UVR reaching the Earth occurs as UVA ( nm) and UVB ( nm), although these wavelengths are only a small percentage of the total solar spectrum. The balance includes mid-range wavelengths of Photosynthetically Active Radiation (PAR), also called visible radiation, used in photosynthesis in algae and plants, and in vision in animals; and longwavelength infrared radiation, IR, manifested as heat. The shorter UVB wavelengths are the least abundant because most have been removed by Earth s protective ozone layer. But UVB radiation contains much energy per photon (Figure 1), so a little UVB goes a long way in damaging tissues by exciting and altering biomolecules when it strikes them; the genetic material in cells, DNA, is especially at risk, as are enzymes and other proteins. The shortest of the UVA wavelengths also are very energetic and may indirectly damage tissues through their interaction with molecular oxygen (O 2), which forms Reactive Oxygen Species (ROS) such as toxic peroxides and free radicals that damage membranes and other cellular components. Figure 1: The energy content of each photon of solar radiation is inversely related to its wavelength. Highly energetic, short-wavelength UVC radiation does not reach the Earth because it interacts with atmospheric components for example with O2 to form the ozone (O3) layer that in turn keeps most solar UVB radiation from reaching us. Modified from Shick, 2007 [7]. Suspicions that UVR can harm corals date back to the early 20 th century but experiments were not undertaken in the field until the 1980s. Corals transplanted from deep (>10 m) to shallow water or to aquaria on the shore under full sunlight died, but not if shielded by UV-opaque glass or acrylic plastic that

3 removed UVR yet allowed longer PAR wavelengths to pass. Sublethal effects of UVR included depressing skeletal growth in corals by lowering their rate of calcification, and inhibiting photosynthesis in their zooxanthellae. In general, corals living in shallower water were less sensitive to UVR than were corals of the same species brought to the surface from deeper water. In the 1960s Japanese scientists found strongly UV-absorbing compounds in red seaweeds, and Kazuo Shibata observed that extracts of symbiotic corals also absorbed strongly around 320 nm (in the UVB/UVA spectrum) because they contained a suite of compounds each differing slightly in their chemical structure and thus the wavelength that they maximally absorbed. These S-320 compounds were more concentrated in corals from shallow water than those living in deeper water or in shaded locations, and in the early 1980s Paul Jokiel and Richard York showed under natural sunlight that the S-320 concentration changed depending on UV-exposure. Together with the different UV-sensitivity of deep- and shallow-living corals, these results suggested a UV-protective role of S-320 compounds in shallow water. Figure 2: Specimens of Stylophora pistillata cultured for years in the aquaria at the Centre Scientifique de Monaco had never been exposed to UVR. Extracts of such corals on day 0 of an experiment showed only traces of UV-absorbing compounds. Acute experimental exposure to broadband UVA + UVB in the presence of PAR elicited the production of materials absorbing at ~327 nm in the corals during 15 days. Control corals in the same aquarium but shielded from UVR for 16 days did not accumulate UV-absorbing materials. The peaks at 664 nm and between 400 and 500 nm are algal chlorophyll and accessory pigments. From Shick et al., 1999 [11]. By comparison with materials from terrestrial fungal spores (mycosporines), S-320 substances in corals were shown by Walter Dunlap and Bruce Chalker to be a suite of similar molecules collectively called mycosporine-like amino acids, or MAAs, which vary individually in their chemical structures and thus in their wavelengths of maximum absorption ( max). Although MAAs strongly absorb UVR (note their collective absorbance peak at 327 nm in Figure 2), they are transparent to PAR and so do not interfere with photosynthesis. MAAs are therefore colorless and not pigments, and do not contribute to the beautiful colors of corals.

4 Figure 3: The core structure of diverse MAAs. R represents chemical substitutions on the central ring that modify the molecule s composition and thus its max. To date, about 20 different MAAs have been identified. By containing multiple MAAs, each having a slightly different max, a coral has a broadband filter that collectively intercepts a wide range of UVA and UVB wavelengths before they damage cellular components. From Shick, 2007 [7]. Because MAAs apparently were synthesized via the shikimate pathway that is present in fungi and algae but absent from animals (such as the coral host), a longtime assumption has been that the symbiotic algae were the source of MAAs in corals; later experiments using inhibitors of the shikimate pathway confirmed its involvement in coral MAA biosynthesis. Thus, a further benefit to the host coral beyond organic nutrition from the algae would be their provision of UV protection, i.e., natural sunscreens. But when MAA concentrations were measured in the entire coral and in zooxanthellae isolated from the colony, concentrations were far higher in the animal (see Figure A in Box 1), and specifically in its ectodermal (outer) tissue. From a sun-screening perspective, this localization makes sense because the surface ectoderm is the first place that sunlight strikes a coral. By concentrating the MAAs there, both the host and the algae deeper in its tissues are protected from UVR (Figure B in Box 1) because these wavelengths are intercepted before they reach critical cellular targets. MAAs are particularly well suited as sunscreens inside the coral s cells because they absorb energetic solar UVR and dissipate the energy harmlessly as heat, rather than forming chemically reactive intermediates that might be toxic to cells. Certain MAAs also act as antioxidants to protect against ROS, another consideration in preventing damage from sunlight. Not only the concentration but also the molecular diversity of MAAs is greater in the coral colony than in the isolated algae, and zooxanthellae raised in culture produce no or only a few MAAs, which together seem inconsistent with MAAs being products of the algal symbionts. The advent of genomic and proteomic technologies allowed the discovery by Walter Dunlap, Paul Long, and colleagues [5, 13] that although the shikimate pathway enzymes involved in making the precursors to MAAs are indeed localized in the algae, the biosynthesis may be completed in the animal cells by other enzymes specific to the host and not found in the algae. Thus, in the coral symbiosis that has evolved over millions of years to thrive in sunlight, the production of UV sunscreens that enable solar exposure is a shared metabolic adaptation between the algal and animal partners. Our experiments at the Centre Scientifique de Monaco indicate that the diverse array of MAAs in corals (up to 10 in Stylophora pistillata) results from the host s converting simple primary MAAs to more complex secondary MAAs having greater stability, less acidity, and wider UV absorption [6, 11, 12].

5 Box 1: MAAs concentrated in the coral host protect it and the algal endosymbionts from UVR The role of MAAs in UV-photoprotection in corals can be tested experimentally. Like the acroporid corals studied earlier by Walter Dunlap, Bruce Chalker, and James Oliver, colonies of Acropora microphthalma have high concentrations of MAAs when growing in shallow water, with MAAs decreasing sharply in deep water (Figure A). Colonies moved from deep to shallow water will experience acutely higher levels of solar UVR, which should exert negative effects on the transplanted deep corals having low concentrations of UV sunscreens. Figure A: Concentrations of natural UV sunscreens mycosporine-like amino acids (MAAs, nanomoles per milligram of protein) in Acropora microphthalma living at different depths. Shown are MAA concentrations in the entire coral colony (host + zooxanthellae, grey bars) and in freshly isolated zooxanthellae (FIZ, black bars) from the same colonies. Data from Shick et al., 1995 [9]. Photo a: Divers from the Australian Institute of Marine Science position an apparatus to measure the photosynthesis in a coral colony placed in the plastic chamber at left. Duplicate apparatuses having chambers made of UV-Opaque or UV-Transparent Plexiglas were deployed at 1 m depth in full sunlight. Corals collected from various depths and placed in the UVT chamber experienced the full solar spectrum, whereas those put in the UVO chamber were shielded specifically from UVR. Results of such experiments are shown in Figure B. Photo: J.M. Shick.

6 Colonies of Acropora microphthalma from deep water (20-30 m) live at low ambient levels of UVR but experienced high levels when acutely transferred to the UV-Transparent chamber at a depth of 1 m (Photo a). As shown in Figure B, compared with deep colonies placed in the UV-Opaque chamber and thus shielded from UVR at 1 m, those in the UVT chamber showed a large UV-inhibition of peak rates of photosynthesis (measured as O2 production per milligram of chlorophyll). Corals living in shallower water (2-10 m) routinely experience higher levels of UVR, which did not affect their photosynthesis. These results are consistent with the greater concentrations of protective MAAs in the corals from 2 m and 10 m (Figure A). Depth Figure B: Peak rates of photosynthesis in colonies of Acropora microphthalma growing at different depths transplanted to 1 m and placed in UV-Opaque (yellow bars) or UV-Transparent (purple bars) chambers in full sunlight. Significant inhibition of photosynthesis by UVR (in the UVT chambers) occurred only in corals originating from 20 m and 30 m. Data from Shick et al., 1995 [9]. Of course the finding of a class of natural UV sunscreens in marine organisms has been of great interest to the cosmetics and cosmeceutical industries. Thus far MAAs have not been synthesized in the laboratory, but some companies have put natural MAAs extracted from sustainably harvested seaweeds into skin care products. For more information: (* = review, where references to the early literature can be found, including the classic studies mentioned in this Factsheet): [1] *Carreto J.I. & Carignan M.O., Mycosporine-like amino acids: Relevant secondary metabolites. Chemical and ecological aspects. Marine Drugs, 9: ; doi: /md [2] *De Mora S., Demers S. & Vernet M. (eds.) The Effects of UV Radiation in the Marine Environment. Cambridge University Press, Cambridge, UK, x+ 324 p.

7 [3] *Dunlap W.C. & Shick J.M., Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. Journal of Phycology, 34: [4] *Karentz D., Chemical defenses of marine organisms against solar radiation exposure: UVabsorbing mycosporine-like amino acids and scytonemin. In: Marine Chemical Ecology, J.B. McClintock & B.J. Baker (eds.), p CRC Press, Boca Raton, FL. [5] Pope M.A., Spence E., Seralvo V., Gacesa R., Heidelberger S., Weston A.J., Dunlap W.C., Shick J.M. & Long P.F., O-methyltransferase is shared between the pentose phosphate and shikimate pathways and is essential for mycosporine-like amino acid biosynthesis in Anabaena variabilis ATCC ChemBioChem, 16: ; doi: /cbc [6] Shick J.M., The continuity and intensity of ultraviolet radiation affect the kinetics of biosynthesis, accumulation, and conversion of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Limnology and Oceanography, 49: [7] *Shick J.M Ultraviolet stress. In: Encyclopedia of Tidepools and Rocky Shores, M.W. Denny & S.D. Gaines (eds.), p University of California Press, Berkeley [8] *Shick J.M. & W.C. Dunlap W.C., Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annual Review of Physiology, 64: [9] Shick J.M., Lesser M.P., Dunlap W.C., Stochaj W.R., Chalker B.E. and Wu Won J., Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Marine Biology, 122: [10] *Shick J.M., Lesser M.P. & Jokiel P.L., Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biology, 2: [11] Shick J.M., Romaine-Lioud S., Ferrier-Pagès C. & Gattuso J.-P., Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnology and Oceanography, 44: [12] Shick J.M., Ferrier-Pagès C. & Grover R. & Allemand D., Effects of starvation, ammonium concentration, and photosynthesis on the UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Marine Ecology Progress Series, 295: [13] Starcevic A., Dunlap W.C., Cullum J., Shick J.M., Hranueli D. & Long P.F., Gene expression in the scleractinian Acropora microphthalma exposed to high solar irradiance reveals elements of photoprotection and coral bleaching. PLoS ONE, 5 (11): e13975 Web sites: [14] [15] [16] [17] [18] Factsheets of Institut océanographique: > L Institut et la science > Fiches scientifiques: [19] Christine Ferrier-Pagès, December 2014: Les coraux scléractiniaires de Méditerranée [20] Jean Jaubert, April 2013: Les récifs coralliens