Cellular responses in the coral Stylophora pistillata exposed to eutrophication from fish mariculture

Evolutionary Ecology Research

Volumn 11, Issue 3, 2009, Pages 381-401

  Kramarsky Winter, E ^a   Downs, C A ^b   Downs, A ^c   Loya, Y ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b Haereticus Environmental Laboratory   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

Biomarkers; Cellular diagnostics; Coral; Fish farm; Gulf of Aqaba (Eilat)

Indexed keywords

ALGAE; ANTHOZOA; SCLERACTINIA; STYLOPHORA PISTILLATA;

EID: 67650320893     PISSN: 15220613     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Atkinson, M.J., Birk, Y. and Rosenthal, H. 2001. Evaluation of pollution in the Gulf of Eilat. Report for the Ministries of Infrastructure, Environment and Agriculture, prepared by the International Expert Team (IET).
2. Atkinson, S. and Atkinson, M.J. 1992. Detection of estradiol-17b during a mass coral spawn. Coral Reefs, 11: 33-35.
3. Baker, A.C., Starger, C.J., McClanahan, T.R. and Glynn, P.W. 2004. Coral reef: coral's adaptive response to climate change. Nature, 430: 741.
4. Bassim, K.M. and Sammarco, P.W. 2003. Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diploria strigosa). Mar. Biol., 142: 241-252. (Pubitemid 36704486)
5. Bongiorni, L., Shafir, S., Angel, D. and Rinkevich, B. 2003a. Survival, growth and reproduction of two hermatypic corals subjected to in situ fish-farm nutrient enrichment. Mar. Ecol. Progr. Ser., 253: 137-144. (Pubitemid 36708524)
6. Bongiorni, L., Shafir, S. and Rinkevich, B. 2003b. Effects of particulate matter released by a fish farm (Eilat, Red Sea) on survival and growth of Stylophora pistillata coral nubbins. Mar. Pollut. Bull., 46: 1120-1124. (Pubitemid 36970195)
7. Bouhouche-Chatelier, L., Chadli, A. and Catelli, M.G. 2001. The N-terminal adenosine triphosphate binding domain of Hsp90 is necessary and sufficient for interaction with estrogen receptor. Cell Stress Chaperones, 6: 297-305. (Pubitemid 33123482)
8. Bowler, C., Van Montagu, M. and Inze, D. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Molec. Biol., 43: 83-116.
9. Brown, B.E. 1997. Coral bleaching: causes and consequences. Coral Reefs, 16: 129-138.
10. Bruno, J.F., Peters, L.E., Harvell, C.D. and Hettinger, A. 2003. Nutrient enrichment can increase the severity of coral disease Ecol. Lett., 6: 1056-1061. (Pubitemid 37537826)
11. Bucher, D.J. and Harrison, P.L. 2002. Growth response of the reef coral Acropora longicyathus to elevated inorganic nutrients: do responses to nutrients vary among coral taxa? Proc. 9th Int. Coral Reef Symp., Bali, 1: 443-448.
12. Buchner, J. 1999. Hsp90 and Co.: a holding for folding. Trends Biochem. Sci., 24: 136-141.
13. Coll, J.C., Bowden, B.F., Carroll, A.R., Tapiolas, D.M., Alino, P.M., Heaton, A. et al. 1994. Chemical aspects of mass spawning corals, I. Sperm attractant molecules in the egg of the scleractinian coral Montipora digitata. Mar. Biol., 48: 177-182. (Pubitemid 2068614)
14. Costa, O.S., Jr., Leão, Z.M.A.N., Nimmo, M. and Attrill, M.J. 2000. Nutrification impacts on coral reefs from northern Bahia, Brazil. Hydrobiologia, 440: 307-315. (Pubitemid 32228543)
15. Cox, E.F. and Ward, S. 2003. Impact of elevated ammonium on reproduction in two Hawaiian scleractinian corals with different life history patterns. Mar. Pollut. Bull., 44: 1230-1235.
16. Crowther, J.R. 2000. The ELISA Guidebook: Theory and Practice. Methods in Molecular Biology #149. Totowa, NJ: Humana Press.
17. Cullen, J.J., Weydert, C., Hinkhouse, M.M., Ritchie, J., Domann, F.E., Spitz, D. et al. 2003. The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma. Cancer Res., 63: 1297-1303. (Pubitemid 36348708)
18. Downs, C.A. 2005. Cellular diagnostics and its application to aquatic and marine toxicology. In Techniques in Aquatic Toxicology, Vol.2 (G. Ostrander, ed.), pp. 181-207. Boca Raton, FL: CRC Press.
19. Downs, C.A., Muller, E., Phillips, S., Fauth, J.E. and Woodley, C.M. 2000. A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar. Biotechnol., 2: 533-544. (Pubitemid 32140026)
20. Downs, C.A., Fauth, J.E. and Woodley, C.M. 2001. Assessing the health of grass shrimp (Palaeomonetes pugio) exposed to natural and anthropogenic stressors: a molecular biomarker system. Mar. Biotechnol., 3: 380-397. (Pubitemid 32925894)
21. Downs, C.A., Fauth, J.E., Halas, J.C., Dustan, P., Bemiss, J. and Woodley, C.M. 2002. Oxidative stress and seasonal coral bleaching Free Radical Biol. Med., 4: 533-543. (Pubitemid 34874974)
22. Dunkov, B.C., Guzov, V.M., Mocelin, G., Shotkoski, F., Brun, A., Amichot, M. et al. 1997. The Drosophila cytochrome P450 gene CYP6a2: structure, localization, heterologous expression, and induction by phenobarbitol. DNA Cell Biol., 16: 1345-1356. (Pubitemid 28006979)
23. Ellis, R.J. 1996. Stress proteins as molecular chaperones. In Stress Proteins in Medicine (W. Van Eden and D.B. Young, eds.), pp. 1-26. New York: Marcel Dekker.
24. Feng, W., Cai, J., Pierce, W.M., Franklin, R.B., Maret, W., Benz, F.W. et al. 2005. Metallothionein transfers zinc to mitochondrial aconitase through a direct interaction in mouse hearts. Biochem. Biophys. Res. Commun., 332: 853-858. (Pubitemid 40745191)
25. Ferrirer-Pagès, C., Gattuso, C., Dallot, S. and Jaubert, J. 2000. The effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs, 19: 103-113. (Pubitemid 30610808)
26. Garcia, E., Ramos, R. and Bastidas, C. 2005. Presence of cytochrome P 450 in the Caribbean corals Sideratsrea siderea and Montastrea faevolata. Ciencias Marinas, 31 (1A): 23-30. (Pubitemid 40383095)
27. Gassman, N.J. and Kennedy, C.J. 1992. Characterization of cytochrome P-450 and xenobiotic metabolizing enzyme activities in the scleractinian coral, Favia fragum. Bull. Mar. Sci., 50: 320-330.
28. Ghosh, S., Gepstein, S., Heikkila, J.J. and Dumbroff, B.G. 1988. Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissue. Analyt. Biochem., 169: 227-233. (Pubitemid 18081397)
29. Goldstone, J.V. 2008. Environmental sensing and response genes in cnidaria: the chemical defensome in the sea anemone Nematostella vectensis. Cell Biol. Toxicol., 24: 483-502.
30. Grasso, L.C., Hayward, D.C., Trueman, J.W., Hardie, K.M., Janssens, P.A. and Ball, E.E. 2001. The evolution of nuclear receptors: evidence from the coral Acropora. Molec. Phylogenet. Evol., 21: 93-102. (Pubitemid 32978505)
31. Hartl, F.U. 1996. Molecular chaperones in cellular protein folding. Nature, 381: 571-579.
32. Hemmingsen, S.M. 1990. The plastid chaperonin. Sem. Cell Biol., 11: 47-54.
33. Honkakoski, P. and Negishi, M. 2000. Regulation of cytochrome P450 (CYP) genes by nuclear receptors. Biochem. J., 347 (Pt. 2): 321-337. (Pubitemid 30229378)
34. Israel National Monitoring for Eilat. 2004. Report available at: http://www.iui-eilat.ac.il/NMP/.
35. Jacob, S.T., Majumder, S. and Ghoshal, K. 2002. Suppression of metallothionein-I/II expression and its probable molecular mechanisms. Environ. Health Perspect., 110 (suppl. 5): 827-830. (Pubitemid 35276875)
36. Kinsey, D.W. and Davies, P.J. 1979. Effects of elevated nitrogen and phosphorus on coral reef growth. Limnol. Oceanogr., 24: 935-940. (Pubitemid 10258216)
37. Klaassen, C.D., Liu, J. and Choudhuri, S. 1999. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol., 39: 267-294. (Pubitemid 29222560)
38. Koop, K., Booth, D., Broadbent, A.D., Brodie, J., Bucher, D., Capone, D. et al. 2001. ENCORE: the effect of nutrient enrichment on coral reefs; synthesis of results and conclusions. Mar. Pollut. Bull., 42: 91-120. (Pubitemid 32178225)
39. Lange, B.M.H., Backi, A., Wilm, M. and Gonzalez, C. 2000. Hsp90 is a core centrosomal component and is required at different stages of the centrosome cycle in Drosophila and vertebrates. EMBO J., 19: 1252-1262. (Pubitemid 30151021)
40. Levy, O., Achituv, Y., Yacobi, Y.Z., Dubinsky, Z. and Stambler, N. 2006. Diel 'tuning' of coral metabolism: physiological response to light cues. J. Exp. Biol., 209: 273-283. (Pubitemid 43226750)
41. Lieber, C.S. 1997. Cytochrome P-450 2E1: its physiological and pathological role. Physiol. Rev., 77: 517-544. (Pubitemid 27184347)
42. Loya, Y. 2004. The coral reefs of Eilat - past, present and future: three decades of coral community structure studies. In Coral Health and Disease (E. Rosenberg and Y. Loya, eds.), pp. 1-34. Berlin: Springer.
43. Loya, Y. 2007. How to influence environmental decision makers? The case of Eilat (Red Sea) coral reefs. J. Exp. Mar. Biol. Ecol., 344: 35-53. (Pubitemid 46454300)
44. Loya, Y., Lubinevsky, H., Rosenfeld, M. and Kramarsky-Winter, E. 2004. Nutrient enrichment caused by in situ fish-farms at Eilat Red Sea is detrimental to coral reproduction. Mar. Pollut. Bull., 49: 344-353. (Pubitemid 39078105)
45. Marubini, F. and Atkinson, M.J. 1999. Effects of lowered pH and elevated nitrate on coral calcification. Mar. Ecol. Progr. Ser., 188: 117-121.
46. Pacey, A.A. and Bentley, M.G. 1992. The fatty acid 8,11,14-eicosatrienoic acid induces spawning in the male lugworm Arenicola marina. J. Exp. Biol., 173: 165-179.
47. Pearl, L.H. and Prodromou, C. 2000. Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol., 10: 46-51. (Pubitemid 30099326)
48. Pernet, V. and Anctil, M. 2002. Annual variations and sex-related differences of estradiol-17â levels in the anthozoan Renilla koellikeri. Gen. Comp. Endocrinol., 129: 63-68.
49. Pratt, W.B. and Dittmar, K.D. 1998. Studies with purified chaperones advance the understanding of the mechanism of glucocorticoid receptor-Hsp90 heterocomplex assembly. Trends Endocrinol. Metab., 9: 244-252. (Pubitemid 28357616)
50. Rinkevich, B. and Loya, Y. 1979. The reproduction of the Red Sea coral Stylophora pistillata. I. Gonads and planulae. Mar. Ecol. Progr. Ser., 1: 133-144.
51. Ronis, M.J.J., Lindros, K.O. and Ingelmann-Sundberg, M. 1996. The CYP2E family. In Cytochrome P450: Metabolic and Toxicological Aspects (C. Ionnides, ed.), pp. 211-239. Boca Raton, FL: CRC Press.
52. Rossi, S., Snyder, M.J. and Gili, J.-M. 2006. Protein, carbohydrate, lipid concentrations and Hsp 70-90 (stress protein) expression over an annual cycle: useful tools to detect feeding constraints in a benthic suspension feeder. Helgol. Mar. Res., 60: 7-17. (Pubitemid 43362033)
53. Rutherford, S.L. and Lindquist, S. 1998. Hsp90 as a capacitor for morphological evolution. Nature, 396: 336-342. (Pubitemid 28557387)
54. Santos, M.M., Hallers-Tjabbes, C.C., Vieira, N., Boon, J.P. and Porte, C. 2002. Cytochrome P450 differences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea. Mar. Environ. Res., 54: 661-665. (Pubitemid 35286491)
55. Scott, J.G. and Wen, Z. 2001. Cytochrome P450 of insects: the tip of the iceberg. Pest Mange. Sci., 57: 958-967. (Pubitemid 32979918)
56. Senft, A.P., Dalton, T.P., Nebert, D.W., Genter, M.B., Puga, A., Hutchinson, R.J. et al. 2002. Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radical Biol. Med., 33: 1268-1278. (Pubitemid 35246595)
57. Sies, H. 1999. Glutathione and its role in cellular functions. Free Radical Biol. Med., 27: 916-921. (Pubitemid 29507465)
58. Simpkins, C., Lloyd, T., Li, S. and Balderman, S. 1998. Metallothionein-induced increase in mitochondrial inner membrane permeability. J. Surg. Res., 75: 30-34. (Pubitemid 28247109)
59. Slattery, M., Hines, G.A. and Watts, S.A. 1997. Steroid metabolism in Antarctic soft corals. Polar Biol., 18: 76-82. (Pubitemid 27268834)
60. Slattery, M., Hines, G.A., Starmer, J. and Paul, V.J. 1999. Chemical signals in gametogenesis, spawning, and larval settlement and defense of the soft coral Sinularia polydactyla. Coral Reefs, 18: 75-84. (Pubitemid 29358026)
61. Snyder, N.J. 2000. Cytochrome P450 enzymes in aquatic invertebrates: recent advances and future directions. Aquatic Toxicol., 48: 529-547.
62. Sokal, R.R. and Rohlf, F.J. 1995. Biometry (pp. 451-499). New York: W.H. Freeman.
63. Stambler, N., Popper, N., Dubinsky, Z. and Stimson, J. 1991. Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis. Pacific Sci., 45: 299-307.
64. Stein, P.C., Ha, T.J. and Parsons, C.L. 2001. Estrogenic regulation of HSP90 kD synthesis in rat urinary bladder. Urological Res., 29: 338-344. (Pubitemid 33051777)
65. Tarrant, A.M. 2005. Endocrine-like signaling in cnidarians: current understanding and implications for ecophysiology. Integr. Comp. Biol., 45: 201-214. (Pubitemid 40748116)
66. Tarrant, A.M., Atkinson, S. and Atkinson, M.J. 1999. Estrone and estradiol-17â concentration in tissue of the scleractinian coral, Montipora verrucosa. Comp. Biochem. Physiol. A: Molec. Integr. Physiol., 122: 85-92. (Pubitemid 29118249)
67. Tarrant, A.M., Blomquist, C.H., Lima, P.H., Atkinson, M.J. and Atkinson, S. 2003. Metabolism of estrogens and androgens by scleractinian corals. Comp. Biochem. Physiol. B: Biochem. Molec. Biol., 136: 473-485. (Pubitemid 37352967)
68. Tarrant, A.M., Reitzel, A.M., Blomquist, C.H., Haller, F., Tokarz, J. and Adamski, J. 2008. Steroid metabolism in cnidarians: Insights from Nematostella vectensis. Molec. Cell. Endocrinol., 24: 56-60.
69. Twan, W.-H., Hwang, J.-.S. and Chang, C.-F. 2003. Sex steroids in scleractinian coral, Euphyllia ancora: implication in mass spawning. Biol. Reproduct., 68: 2255-2260. (Pubitemid 36687019)
70. Twan, W.-H., Hwang, J.-S., Lee, Y.-H., Wu, H.-F., Tung, Y.-H. and Chang, C.-F. 2006. Hormones and reproduction in scleractinian corals. Comp. Biochem. Physiol. A: Molec. Integr. Physiol., 144: 247-253. (Pubitemid 43956564)
71. Ye, B., Maret, W. and Vallee, B.L. 2001. Zinc metallothionein imported into liver mitochondria modulates respiration. Proc. Natl. Acad. Sci. USA, 98: 2317-2322. (Pubitemid 32209480)
72. Zvuloni, A. 2003. Intra-specific genetic variability of the corals Stylophora pistillata and Heteroxenia fuscescens from the northern tip of the Gulf of Eilat. MSc thesis, Tel Aviv University (in Hebrew with English abstract).