Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1648, 2008, Pages 2273-2282

  Abrego, David ^a,b   Ulstrup, Karin E ^b,c   Willis, Bette L ^a   Van Oppen, Madeleine J H ^b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Coral bleaching; Heat stress; Oxygen consumption and respiration; Photosystem II; Symbiodinium; Xanthophylls

Indexed keywords

CHLOROPHYLL A; OXYGEN; PIGMENT;

ALGA; BLEACHING; COMPARATIVE STUDY; CORAL; CORAL BLEACHING; ENDOSYMBIONT; INTERSPECIFIC INTERACTION; JUVENILE; LIGHT EFFECT; OXYGEN CONSUMPTION; PHOTOSYNTHESIS; PHYSIOLOGY; PIGMENT; RESPIRATION; SYMBIOSIS; TOLERANCE; WARMING;

ALGA; ARTICLE; BLEACHING; BREATHING; CONTROLLED STUDY; CORAL; ENDOSYMBIONT; FLUORESCENCE; HEAT STRESS; HEAT TOLERANCE; JUVENILE; LIGHT STRESS; METABOLISM; NONHUMAN; PRIORITY JOURNAL; SPECIES DIFFERENCE;

ACROPORA MILLEPORA; ACROPORA TENUIS; ALGAE; ANTHOZOA; SYMBIODINIUM;

EID: 49749096808     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0180     Document Type: Article

References (59)

1. Ambarsari, I., Brown, B. E., Barlow, R. G., Britton, G. & Cummings, D. G. 1997 Fluctuations in algal chlorophyll and carotenoid pigments during solar bleaching in the coral Goniastrea aspera at Phuket, Thailand. Mar. Ecol. Prog. Ser. 159, 303-307. (doi:10.3354/meps159303)
2. Baird, A. H. & Marshall, P. A. 2002 Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 237, 133-141. (doi:10.3354/meps237133)
3. Baker, A. C. 2001 Reef corals bleach to survive change. Nature 411, 765-766. (doi:10.1038/35081151)
4. Baker, A. C. 2003 Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661-689. (doi:10.1146/annurev.ecolsys.34.011802.132417)
5. Baker, A. C., Starger, C., McClanahan, T. & Glynn, P. W. 2004 Coral's adaptive response to climate change. Nature 430, 741. (doi:10.1038/430741a)
6. Berkelmans, R. & van Oppen, M. J. H. 2006 The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc.R. Soc. B 273, 2305-2312. (doi:10.1098/rspb.2006.3567)
7. Bhagooli, R. & Hidaka,M. 2003 Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. J. Exp. Mar. Biol. Ecol. 291, 181-197.
8. Brown, B. E. 1997 Coral bleaching: causes and consequences. Coral Reefs 16, 129-138. (doi:10.1007/s003380050249)
9. Brown, B. E., Ambarsari, I., Warner, M. E., Fitt, W. K., Dunne, R. P., Gibb, S. W. & Cummings, D. G. 1999 Diurnal changes in photochemical efficiency and xanthopyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18, 99-105. (doi:10.1007/s003380050163)
10. Brown, B. E., Downs, C. A., Dunne, R. P. & Gibb, S. W. 2002 Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 242, 119-129. (doi:10.3354/meps242119)
11. Buddemeier, R. W. & Fautin, D. G. 1993 Coral bleaching as an adaptive mechanism. Bioscience 43, 320-326. (doi:10.2307/1312064)
12. Coffroth, M. A. & Santos, S. R. 2005 Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156, 19-34. (doi:10.1016/j.protis.2005.02.004)
13. Downs, C. A., Mueller, E., Phillips, S., Fauth, J. & Woodley, C. 2000 Amolecular biomarker systemfor assessing the health of coral (Montastrea faveolata) during heat stress. Mar. Biotechnol. 2, 533-544. (doi:10.1007/s101260000038)
14. Dunlap, W. C. & Shick, J. M. 1998 Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. Coral Reefs 20, 201-210.
15. Enriquez, S. 2005 Light absorption efficiency and the package effect in the leaves of the seagrass Thalassia testudinum. Mar. Ecol. Prog. Ser. 289, 141-150. (doi:10.3354/meps289141)
16. Enriquez, S., Mendez, E. R. & Iglesias-Prieto, R. 2005 Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50, 1025-1032.
17. Epping, E. & Kühl, M. 2000 The responses of photosynthesis and oxygen consumption to short-term changes in temperature and irradiance in a cyanobacterial mat (Ebro Delta, Spain). Environ. Microbiol. 2, 465-474. (doi:10.1046/j.1462-2920.2000.00129.x)
18. Fabricius, K. E., Mieog, J. C., Colin, P. L., Idip, D. & van Oppen, M. J. H. 2004 Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13, 2445-2458. (doi:10.1111/j.1365-294X. 2004.02230.x)
19. Fitt, W. K. 1985 Effect of different strains of the zooxanthella Symbiodinium microadriaticum on growth and survival of their coelenterate and molluscan hosts. In Proc. 5th Int. Coral Reef Congress, Tahiti, French Polynesia, pp. 131-136.
20. Fitt, W. K., Brown, B. E., Warner, M. E. & Dunne, R. P. 2001 Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51-65. (doi:10.1007/ s003380100146)
21. Glynn, P. W., Mate, J. L., Baker, A. & Calderon, M. O. 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.
22. Gorbunov, M. Y., Kolber, Z., Lesser, M. P. & Falkowski, P. G. 2001 Photosynthesis and photoprotection in symbiotic corals. Limnol. Oceanogr. 46, 75-85.
23. Goulet, T. L. 2006 Most corals may not change their symbionts. Mar. Ecol. Prog. Ser. 321, 1-7. (doi:10.3354/meps321001)
24. Goulet, T. L., Cook, C. B. & Goulet, D. 2005 Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallidal Symbiodinium symbiosis. Limnol. Oceanogr. 50, 1490-1498.
25. Hoegh-Guldberg, O. 1999 Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50, 839-866. (doi:10.1071/MF99078)
26. Hughes, T. P. et al. 2003 Climate change, human impacts, and the resilience of coral reefs. Science 301, 929. (doi:10.1126/science. 1085046)
27. Iglesias-Prieto, R. & Trench, R. K. 1994 Acclimation and adaptation to irradiance in symbiotic dinoflagellates. 1. Responses of the photosynthetic unit to changes in photon flux density. Mar. Ecol. Prog. Ser. 113, 163-175. (doi:10.3354/meps113163)
28. Iglesias-Prieto, R. & Trench, R. K. 1997 Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbioses. In Proc. 8th Int. Coral Reef Symp. pp. 1319-1324. Panama City, Panama: Smithsonian Tropical Research Institute.
29. Iglesias-Prieto, R., Beltrán, V. H., LaJeunesse, T. C., Reyes-Bonilla, H. & Thomé, P. E. 2004 Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc. R. Soc. B 271, 1757-1763. (doi:10.1098/rspb.2004. 2757)
30. 2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21, 1219-1230. (doi:10.1046/j.1365-3040.1998.00345.x)
31. Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. 2008 A community shift in the symbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. R. Soc. B 275, 1359-1365. (doi:10.1098/rspb.2008.0069)
32. Jones, A. M., Cantin, N. E., Berkelmans, R., Sinclair, B. & Negri, A. P. 2008 A 3D modeling method to calculate the surface areas of coral branches. Coral Reefs 27, 521-526. (doi:10.1007/s00338-008-0354-y)
33. 2, pH and light. Mar. Ecol. Prog. Ser. 117, 159-172. (doi:10.3354/meps117159)
34. LaJeunesse, T. C. 2001 Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a "species" level marker. J. Phycol. 37, 866-880. (doi:10.1046/j.1529-8817.2001.01031.x)
35. LaJeunesse, T. C. 2005 "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol. Biol. Evol. 22, 570-581. (doi:10.1093/molbev/ msi042)
36. LaJeunesse, T. C., Loh, W. K., van Woesik, R., Hoegh-Guldberg, O., Schmidt, G. W. & Fitt, W. K. 2003 Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48, 2046-2054.
37. Lesser, M. P. & Farrell, J. H. 2004 Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23, 367-377. (doi:10.1007/s00338-004- 0392-z)
38. Lesser, M. P., Stochaj, W. R., Tapley, D. W. & Shick, J. M. 1990 Bleaching in coral-reef anthozoans: effects of irradiance, ultraviolet- radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8, 225-232. (doi:10.1007/BF00265015)
39. Li, W. K. W., Smith, J. C. & Platt, T. 1984 Temperature response of photosynthetic capacity and carboxylase activity in Arctic marine phytoplankton. Mar. Ecol. Prog. Ser. 17, 237-243. (doi:10.3354/meps017237)
40. Little, A. F., van Oppen, M. J. H. & Willis, B. L. 2004 Flexibility in algal endosymbioses shapes growth in reef corals. Science 304, 1492-1494. (doi:10.1126/science.1095733)
41. Maxwell, D. P., Falk, S. & Huner, N. 1995 Photosystem II excitation pressure and development of resistance to photoinhibition (I. Light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris). Plant Physiol. 107, 687-694.
42. Michalek-Wagner, K. & Willis, B. L. 2001 Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability. Coral Reefs 19, 231-239. (doi:10.1007/ s003380170003)
43. Mieog, J., van Oppen, M. J. H., Cantin, N., Stam, W. T. & Olsen, J. L. 2007 Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26, 449-457. (doi:10.1007/s00338-007-0244-8)
44. Platt, T., Gallegos, C. L. & Harrison, W. G. 1980 Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38, 687-701.
45. Revsbech, N. P. & Jorgensen, B. 1983 Photosynthesis of benthic microflora measured with high spatial resolution by the oxygen microprofile method: capabilities and limitations of the method. Limnol. Oceanogr. 28, 749-756.
46. Robison, J. D. & Warner, M. E. 2006 Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrohphyta). J. Phycol. 42, 568-579. (doi:10.1111/j.1529-8817.2006.00232.x)
47. Rodriguez-Lanetty, M., Krupp, D. A. & Weis, V. M. 2004 Distinct ITS types of Symbiodinium in clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar. Ecol. Prog. Ser. 275, 97-102. (doi:10.3354/meps275097)
48. Rowan, R. 2004 Thermal adaptations in reef coral symbionts. Nature 430, 742. (doi:10.1038/430742a)
49. Rowan, R. & Knowlton, N. 1995 Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc. Natl Acad. Sci. USA 92, 2850-2853. (doi:10.1073/pnas.92.7.2850)
50. Salih, A., Larkum, A., Cox, G., Kühl,M. & Hoegh-Guldberg, O. 2000 Fluorescent pigments in corals are photoprotective. Nature 408, 850-853. (doi:10.1038/35048564)
51. Shick, J. M., Lesser, M. P., Dunlap, W. C., Stochaj, W. R., Chalker, B. E. & Won, J. W. 1995 Depth-dependent responses to solar ultraviolet- radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar. Biol. 122, 41-51. (doi:10.1007/BF00349276)
52. Takahashi, S., Takahashi, N., 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 Environ. 45, 251-255.
53. Tchernov, D., Gorbunov, M. Y., de Vargas, C., Narayan Yadav, S., Milligan, A. J., Haggblom, M. & Falkowski, P. G. 2004 Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl Acad. Sci. USA 101, 13 531-13 535. (doi:10.1073/pnas. 0402907101)
54. Toller, W. W., Rowan, R. & Knowlton, N. 2001 Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol. Bull. 201, 360. (doi:10.2307/1543614)
55. Ulstrup, K. E. & van Oppen, M. J. H. 2003 Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol. Ecol. 12, 3477-3484. (doi:10.1046/j.1365-294X.2003.01988.x)
56. van Oppen, M. J. H., Palstra, F. P., Piquet, A. M.-T. & Miller, D. J. 2001 Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc. R. Soc. B 268, 1759-1767. (doi:10.1098/rspb.2001.1733)
57. van Oppen, M. J. H., Mahiny, A. & Done, T. 2005 Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24, 482-487. (doi:10.1007/s00338-005-0487-1)
58. Warner, M. E., Fitt, W. K. & Schmidt, G. W. 1996 The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ. 19, 291-299. (doi:10.1111/j.1365-3040.1996. tb00251.x)
59. Warner, M. E., Fitt, W. K. & Schmidt, G. W. 1999 Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl Acad. Sci. USA 96, 8007-8012. (doi:10.1073/pnas.96.14. 8007)