Analysis of fluorescent and non-fluorescent sea anemones from the Mediterranean Sea during a bleaching event

Journal of Experimental Marine Biology and Ecology

Volumn 353, Issue 2, 2007, Pages 221-234

  Leutenegger, Alexandra ^a   Kredel, Simone ^a   Gundel, Silke ^a   D'Angelo, Cecilia ^a   Salih, Anya ^b   Wiedenmann, Jörg ^a,c  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF SYDNEY   (Australia)

^c National Oceanography Center   (United Kingdom)

Author keywords

Anthozoa; Bleaching; Fluorescent proteins; GFP; Photoprotection; Zooxanthellae

Indexed keywords

AMINO ACID; BLEACHING; ENZYME ACTIVITY; FLUORESCENCE; INVERTEBRATE; PHYSIOLOGICAL RESPONSE; PIGMENT; PROTEIN; ZOOXANTHELLA;

MEDITERRANEAN SEA;

ACTINIARIA; AEQUOREA VICTORIA; ANEMONE; ANEMONIA; ANEMONIA RUSTICA; ANEMONIA SULCATA; ANIMALIA; ANTHOZOA;

EID: 36248945674     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2007.09.013     Document Type: Article

References (94)

1. Andres A. Prodromus neapolitanae actiniarum faunae. Mitt. Zool. Stn. Neapel 2 (1881) 305-317
2. Banin E., Vassilakos D., Orr E., Martinez R.J., and Rosenberg E. Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr. Microbiol. 46 (2003) 418-422
3. Ben-Haim Y., Thompson F.L., Thompson C.C., Cnockaert M.C., Hoste B., Swings J., and Rosenberg E. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int. J. Syst. Evol. Microbiol. 53 (2003) 309-315
4. Blum H., Beier H., and Gross J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8 (1987) 93-99
5. Bou-Abdallah F., Chasteen N.D., and Lesser M.P. Quenching of superoxide radicals by green fluorescent protein. Biochim. Biophys. Acta 1760 (2006) 1690-1695
6. Brown B.E. Coral bleaching: causes and consequences. Coral Reefs 16 (1997) 129-138
7. Brown B.E., Le Tissier M.D.A., and Bythell J.C. Mechanisms of bleaching deduced from histological studies of reef corals during a natural bleaching event. Mar. Biol. 122 (1995) 655-663
8. Brown B.E., Dunne R., Goodson M., and Douglas A. Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21 (2002) 119-126
9. Bulnheim H.P., and Sauer K.P. Anemonia sulcata-zwei Arten? Genetische und ökologische Evidenz. Verh. Dtsch. Zool. Ges. 77 (1984) 264
10. Burkenroad M.D. A possible function of bioluminescence. J. Mar. Res. 5 (1943) 161-164
11. Coles S.L., and Jokiel P.L. Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar. Biol. 49 (1978) 187-195
12. Coles S., and Brown B. Coral bleaching - capacity for acclimatization and adaptation. Adv. Mar. Biol. 46 (2003) 183-223
13. Cox G., and Salih A. Confocal microscopy of GFP-like pigments in corals. In: Yu H., Cheng P.C., Lin P.C., and Kao F.J. (Eds). Multimodal Microscopy (2006), World Scientific Publishing, Singapore 238-245
14. Cox G., Matz M., and Salih A. Fluorescence lifetime imaging of coral fluorescent proteins. Microsc. Res. Tech. 70 (2006) 243-251
15. Dove S.G. Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar. Ecol. Prog. Ser. 272 (2004) 99-116
16. Dove S.G., Hoegh-Guldberg O., and Ranganathan S. Major colour patterns of reefbuilding corals are due to a family of GFP-like proteins. Coral Reefs 19 (2001) 197-204
17. Downs C.A., Fauth J.E., Halas J.C., Dustan P., Bemiss J., and Woodley C.M. Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 33 (2002) 533-543
18. Dunlap W.C., and Shick J.M. Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J. Phycol. 34 (1998) 418-430
19. Field S.F., Bulina M.Y., Kelmanson I.V., Bielawski J.P., and Matz M.V. Adaptive evolution of multicolored fluorescent proteins in reef-building corals. J. Mol. Evol. 62 (2006) 332-339
20. Fitt W.K., Brown B.E., Warner M.E., and Dunne R.P. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20 (2001) 51-65
21. Gagnon M., Hunting W.M., and Esselen W.B. New method of catalase determination. Anal. Chem. 31 (1959) 144-145
22. Gates R.D., Baghdasarian G., and Muscatine L. Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol. Bull. 182 (1992) 324-332
23. Gilmore A.M., Larkum A.W.D., Salih A., Itoh S., Shibata Y., Bena C., Yamasaki H., Papina M., and van Woesik R. Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem. Photobiol. 77 (2003) 515-523
24. Gleason D.F. Differential effects of ultraviolet radiation on green and brown morphs of the Carribbean coral Porites astreoides. Limnol. Oceanogr. 38 (1993) 1452-1463
25. Glynn P.W. Widespread coral mortality and the 1982/83 El Niño warming event. Environ. Conserv. 11 (1984) 133-146
26. Glynn P.W. Coral-reef bleaching - ecological perspectives. Coral Reefs 12 (1993) 1-17
27. Glynn P.W., and D'Croz L. Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortalities. Coral Reefs 8 (1990) 181-191
28. Goreau T.E. Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Elora. Science 145 (1964) 383-386
29. Goreau T.J., and Hayes R.L. Coral bleaching and ocean 'hot spots'. Ambio 23 (1994) 176-180
30. Gosse P.H., (ed.) 1860. Actinologia Britannica: a history of the british sea-anemones and corals. Van Voorst, Paternoster Row London.
31. Haddock S.H.D., Dunn C.W., Pugh P.R., and Schnitzler C.E. Bioluminescent and red-fluorescent lures in a deep-sea siphonophore. Science 309 (2005) 263
32. Harvell C.D., Kim K., Burkholder J.M., Colwell R.R., Epstein P.R., Grimes D.J., Hofmann E.E., Lipp E.K., Osterhaus A.D.M.E., Overstreet R.M., Porter J.W., Smith G.W., and Vasta G.R. Emerging marine diseases - climate links and anthropogenic factors. Science 285 (1999) 1505-1510
33. Hawkridge J.M., Pipe R.K., and Brown B.E. Localization of antioxidant enzymes in the cnidarians Anemonia viridis and Goniopora stokesi. Mar. Biol. 137 (2000) 1-9
34. 2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen 167 (1975) 191-194
35. Kawaguti S. On the physiology of reef corals VI. Study on the pigments. Palao Trop. Biol. Stn. Stud. 2 (1944) 617-674
36. Kawaguti S. Effect of the green fluorescent pigment on the productivity of reef corals. Micronesia 5 (1969) 313
37. Kelmanson I.V., and Matz M.V. Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). Mol. Biol. Evol. 20 (2003) 1125-1133
38. Kleppel G.S., Dodge R.E., and Reese C.J. Changes in pigmentation associated with the bleaching of stony corals. Limnol. Oceanogr. 34 (1989) 1331-1335
39. Kushmaro A., Loya Y., Fine M., and Rosenberg E. Bacterial infection and coral bleaching. Nature 380 (1996) 396
40. Kushmaro A., Rosenberg E., Fine M., and Loya Y. Bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar. Ecol. Prog. Ser. 147 (1997) 159-165
41. Kushmaro A., Rosenberg E., Fine M., Ben-Haim Y., and Loya Y. Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar. Ecol. Prog. Ser. 171 (1998) 131-137
42. Labas Y.A., Gurskaya N.G., Yanushevich Y.G., Fradkov A.F., Lukyanov K.A., Lukyanov S.A., and Matz M.V. Diversity and evolution of the green fluorescent protein family. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 4256-4261
43. Laemmli K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
44. Lesser M.P. Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnol. Oceanogr. 41 (1996) 271-283
45. Lesser M.P. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16 (1997) 187-192
46. Lesser M.P., and Shick J.M. 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 (1989) 243-255
47. Lesser M.P., Stochaj W.R., Tapley D.W., and Shick J.M. Bleaching in coral reef anthozoans: effects of irradiance, ultra-violet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8 (1990) 225-232
48. Leutenegger, A., D'Angelo, C., Matz, M.V., Denzel, A., Oswald, F., Salih, A., Nienhaus, G.U., Wiedenmann, J. 2007. It's cheap to be colorful: Anthozoans show a slow turnover of GFP-like proteins. FEBS J. 274, 2496-2505.
49. Louis C. Modalités et déterminisme expérimental de la scissiparité chez l'actinie Anemonia sulcata. C. R. hebd Séances Acad Sci, Paris 251 (1960) 134-136
50. Lukyanov K.A., Fradkov A.F., Gurskaya N.G., Matz M.V., Labas Y.A., Savitsky A.P., Markelov M.L., Zaraisky A.G., Zhao X., Fang Y., Tan W., and Lukyanov S.A. Natural animal coloration can be determined by a nonfluorescent green fluorescent protein homolog. J. Biol. Chem. 275 (2000) 25879-25882
51. Martynov V.I., Savitsky A.P., Martynova N.Y., Savitsky P.A., Lukyanov K.A., and Lukyanov S.A. Alternative cyclization in GFP-like proteins family. The formation and structure of the chromophore of a purple chromoprotein from Anemonia sulcata. J. Biol. Chem. 276 (2001) 21012-21016
52. Matz M.V., Fradkov A.F., Labas Y.A., Savitsky A.P., Zaraisky A.G., Markelov M.L., and Lukyanov S.A. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 17 (1999) 969-973
53. Matz M.V., Labas Y.A., and Ugalde J. Evolution of functions and color in GFP-like proteins. In Green Fluorescent Protein: Properties, Applications and Protocolls. 2nd ed. In: Chalfie M., and Kain S.R. (Eds) (2005), Wiley-Liss, New York 110-129
54. Mazel C.H., Lesser M.P., Gorbunov M.Y., Barry T.M., Farrell J.H., Wyman K.D., and Falkowski P.G. Green-fluorescent proteins in Caribbean corals. Limnol. Oceanogr. 48 (2003) 402-411
55. Merle P.L., Sabourault C., Richier S., Allemand D., and Furla P. Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Radic. Biol. Med. (2006) 10.1016/j.freeradbiomed.2006.10.038
56. Miller D., Brown B.E., Sharp V.A., and Nganro N. Changes in the expression of soluble proteins extracted from the symbiotic anemone Anemonia viridis accompany bleaching induced by hyperthermia and metal stressors. J. Therm. Biol. 17 (1992) 217-223
57. Morin J.G. Coelenterate bioluminescence. In: Muscatine L., and Lenhoff H. (Eds). Coelenterate biology: reviews and new perspectives (1974), Academic Press, New York 397-438
58. Muller-Parker G. Effect of feeding regime and irradiance on the photophysiology of the symbiotic sea anemone Aiptasia pulchella. Mar. Biol. 90 (1985) 65-74
59. Muscatine L., Grossman D., and Doino J. Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar. Ecol. Prog. Ser. 77 (1991) 233-243
60. Nienhaus K., Renzi F., Vallone B., Wiedenmann J., and Nienhaus G.U. Chromophore-protein interactions in the anthozoan green fluorescent protein asFP499. Biophys J. 91 (2006) 4210-4220
61. Oswald F., Schmitt F., Leutenegger A., Ivanchenko S., D'Angelo C., Salih A., Maslakova S., Bulina M., Nienhaus G.U., Matz M.V., and Wiedenmann J. Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J. 274 (2007) 1102-1122
62. Plantivaux A., Furla P., Zoccola D., Garello G., Forcioli D., Richier S., Merle P.L., Tambutté E., Tambutté S., and Allemand D. Molecular characterization of two Cu-Zn superoxide dismutases in a sea anemone. Free Radic. Biol. Med. 37 (2004) 1170-1181
63. Pohjanvirta R., Niittynen M., Linden J., Boutros P.C., Moffat I.D., and Okey A.B. Evaluation of various housekeeping genes for their applicability for normalization of mRNA expression in dioxin-treated rats. Chem. Biol. Interact. 160 (2006) 134-149
64. Prasher D.C., Eckenrode V.K., Ward W.W., Prendergast F.G., and Cormier M.J. Primary structure of the Aeqourea victoria green fluorescent protein. Gene 111 (1992) 229-233
65. Pockley P. Global warming could kill most coral reefs by 2100. Nature 400 (1999) 98
66. Pockley P. Global warming identified as main threat to coral reefs. Nature 407 (2000) 932
67. Richier S., Merle P.L., Furla P., Pigozzi D., Sola F., and Allemand D. Characterization of superoxide dismutases in anoxia- and hyperoxia-tolerant symbiotic cnidarians. Biochim. Biophys. Acta 1621 (2003) 84-91
68. Richier S., Furla P., Plantivaux A., Merle P.L., and Allemand D. Symbiosis-induced adaptation to oxidative stress. J. Exp. Biol. 208 (2005) 277-285
69. Richier S., Sabourault C., Courtiade J., Zucchini N., Allemand D., and Furla P. Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J. 273 (2006) 4186-4198
70. Rodolfo-Metalpa R., Richard C., Allemand D., Bianchi C.N., Morri C., and Ferrier-Pagès C. Response of zooxanthellae in symbiosis with the Mediterranean corals Cladocora caespitosa and Oculina patagonica to elevated temperatures. Mar. Biol. 150 (2006) 45-55
71. Salih A., Hoegh-Guldberg O., and Cox G. Photoprotection of symbiotic dinoflagellates by fluorescent pigments in reef corals. In: Greenwood H. (Ed). Proc Aust Coral Reef Society vol. 75 (1998) 217-230 Anniv Conference
72. Salih A., Larkum A., Cox G., Kühl M., and Hoegh-Guldberg O. Fluorescent pigments in corals are photoprotective. Nature 408 (2000) 850-853
73. Salih A., Cox G., Coles S., Baird A., Dunstan A., Mills J., and Larkum A.W.D. Role of coral host-based fluorescent pigments in reducing coral bleaching stress. 2004 10th International Coral Reef Symposium (2006), Okinawa, Japan 12 pages
74. Savage A.M., Goodson M.S., Visram S., Trapido-Rosenthal H., Wiedenmann J., and Douglas A.E. Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar. Ecol. Prog. Ser. 244 (2002) 17-26
75. Schlichter D., Fricke H.W., and Weber W. Light harvesting by wavelength transformation in a symbiotic coral of the Red Sea twilightzone. Mar. Biol. 91 (1986) 403-407
76. Shagin D.A., Barsova E.V., Yanushevich Y.G., Fradkov A.F., Lukyanov K.A., Labas Y.A., Semenova T.N., Ugalde J.A., Meyers A., Nunez J.M., Widder E.A., Lukyanov S.A., and Matz M.V. GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity. Mol. Biol. Evol. 5 (2004) 841-850
77. Shick J.M., and Dykens J.A. Oxygen detoxification in algal-invertebrate symbioses from the Great Barrier Reef. Oecologia 66 (1985) 33-41
78. Shick J.M., Lesser M.P., Dunlap W.C., and Stochaj W.R. Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar. Biol. 122 (1995) 41-51
79. Smith D.J., Suggett D.J., and Baker N.R. Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals?. Glob. Chang. Biol. 11 (2005) 1-11
80. Stochaj W.R., Dunlap W.C., and Shick J.M. Two new UV-absorbing mycosporine-like amino acids from the sea anemone Anthopleura elegantissima and the effects of zooxanthellae and spectral irradiance on chemical composition and content. Mar. Biol. 118 (1994) 149-156
81. Stone L., Huppert A., Rajagopalan B., Bhasin H., and Loya Y. Mass coral reef bleaching: a recent outcome of increased El Niño activity?. Ecol. Lett. 2 (1999) 325-330
82. Tchernov D., Gorbunov M.Y., de Vargas C., Yadav S.N., Milligan A.J., Häggblom M., and Falkowski P.G. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13531-13535
83. Ugalde J.A., Chang B.S., and Matz M.V. Evolution of coral pigments recreated. Science 305 (2004) 1433
84. Visram S., Wiedenmann J., and Douglas A.E. Molecular diversity of symbiotic algae Symbiodinium (Zooxanthellae) in Cnidarians of the Mediterranean Sea. J. Mar. Biol. Assoc. UK 86 (2006) 1281-1283
85. Wiedenmann, J., 1997. Die Anwendung eines orange fluoreszierenden Proteins und weiterer farbiger Proteine und der zugehörenden Gene aus der Artengruppe Anemonia sp. (sulcata) Pennant, (Cnidaria, Anthozoa, Actinaria) in Gentechnologie und Molekularbiologie. Offenlegungsschrift DE 197 18 640 A1. Deutsches Patent-und Markenamt, pp 1-18.
86. Wiedenmann J., Röcker C., and Funke W. The morphs of Anemonia aff. sulcata (Cnidaria, Anthozoa) in particular consideration of the ectodermal pigments. In: Pfadenhauer J. (Ed). Verhandlungen der Gesellschaft für Ökologie, Band vol. 29 (1999), Spektrum Akademischer Verlag, Heidelberg Berlin 497-503
87. Wiedenmann J., Kraus P., Funke W., and Vogel W. The relationship between different morphs of Anemonia sulcata PENNANT (Anthozoa, Actinaria) evaluated by DNA fingerprinting. Ophelia 52 (2000) 57-64
88. Wiedenmann J., Elke C., Spindler K.D., and Funke W. Cracks in the β-can: fluorescent proteins from Anemonia sulcata. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 14091-14096
89. Wiedenmann J., Elke C., Spindler K.D., and Funke W. Correction for vol. 97, pp 14091-14096. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13357 2002
90. Wiedenmann J., Schenk A., Röcker C., Girod A., Spindler K.D., and Nienhaus G.U. A far-red fluorescent protein with fast maturation and reduced oligomerization tendency from Entacmaea quadricolor (Cnidaria, Anthozoa, Actinaria). Proc. Natl. Acad. Sci. 99 (2002) 11646-11651
91. Wiedenmann J., Ivanchenko S., Oswald F., and Nienhaus G.U. Identification of GFP-like proteins in non-bioluminescent, azooxanthellate Anthozoa opens new perspectives for bioprospecting. Mar. Biotechnol. 6 (2004) 270-277
92. Wiedenmann, J., Leutenegger, A., Gundel, S., Schmitt, F., D'Angelo, C., Funke, W., 2007. Long-term monitoring of space competition among fluorescent and nonfluorescent sea anemones in the Mediterranean Sea. J. Mar. Biol. Assoc. UK. 87, 851-852.
93. Wilmann P.G., Petersen J., Devenish R.J., Prescott M., and Rossjohn J. Variations on the GFP chromophore: a polypeptide fragmentation within the chromophore revealed in the 2.1-A crystal structure of a nonfluorescent chromoprotein from Anemonia sulcata. J. Biol. Chem. 280 (2005) 2401-2404
94. Wilson W.H., Francis I., Ryan K., and Davy K. Temperature induction of viruses in symbiotic dinoflagellates. Aquat. Microb. Ecol. 25 (2001) 99-102