Variability in the primary site of photosynthetic damage in symbiodinium sp. (dinophyceae) exposed to thermal stress

Journal of Phycology

Volumn 48, Issue 1, 2012, Pages 117-126

  Buxton, Lucy ^a   Takahashi, Shunichi ^b   Hill, Ross ^a   Ralph, Peter J ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Calvin cycle; Coral bleaching; Pulse amplitude modulated fluorometry; Symbiodinium; Thermal inhibition

Indexed keywords

ANTHOZOA; DINOPHYCEAE; POCILLOPORA DAMICORNIS; SCLERACTINIA; STYLOPHORA PISTILLATA; SYMBIODINIUM; SYMBIODINIUM SP.;

EID: 84856486644     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2011.01099.x     Document Type: Article

References (40)

1. Abrego, D., Ulstrup, K. E., Willis, B. L. & van Oppen, M. J. H. 2008. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc. R. Soc. Lond. B 275:2273-82.
2. Allakhverdieva, S. I. & Murata, N. 2004. Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta 1657:23-32.
3. Baird, A., Bhagooli, R., Ralph, P. J. & Takahashi, S. 2009. Coral bleaching: the role of the host. Trends Ecol. Evol. 24:16-20.
4. Bhagooli, R. & Hidaka, M. 2003. Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. J. Exp. Mar. Biol. Ecol. 291:181-97.
5. Falkowski, P. G. & Raven, J. A. 1997. Aquatic Photosynthesis, 2nd ed. Blackwell science, Malden, Massachusetts, 484 pp.
6. Fitt, W. K. & Warner, M. E. 1995. Bleaching patterns of four species of Caribbean rReef corals. Biol. Bull. 189:298-307.
7. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229-39.
8. Hennige, S. J., Suggett, D. J., Warner, M. E., McDougall, K. E. & Smith, D. J. 2009. Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179-95.
9. Hill, R., Brown, C., DeZeeuw, K., Campbell, D. & Ralph, P. J. 2011. Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation. Limnol. Oceanogr. 56:139-46.
10. Hill, R., Larkum, A. W. D., Frankart, C., Kuhl, M. & Ralph, P. J. 2004. Loss of functional photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics. Photosynth. Res. 82:59-72.
11. Hill, R. & Ralph, P. J. 2005. Diel and seasonal changes in fluorescence rise kinetics of three scleractinian corals. Funct. Plant Biol. 32:549-59.
12. Hill, R., Ulstrup, K. E. & Ralph, P. J. 2009. Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated and expelled zooxanthellae from scleractinian corals. Bull. Mar. Sci. 85:223-44.
13. Hoegh-Guldberg, O. 2011. Coral reef ecosystems and anthropogenic climate change. Reg. Environ. Change 11:S215-27.
14. Iglesias-Prieto, R. 1997. Temperature-dependent inactivation of photosystem II in symbiotic dinoflagellates. Proc. 8th Int. Coral Reef Symp. 2:1313-8.
15. Iglesias-Prieto, R., Matta, J. L., Robins, W. A. & Trench, R. K. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. U. S. A. 89:10302-5.
16. 2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen 167:191-4.
17. 2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21:1219-30.
18. LaJeunesse, T., Loh, W. K. W., van Woesik, R., Hoegh-Guldberg, H., Schmidt, G. W. & Fitt, W. K. 2003. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48:2046-54.
19. Leggat, W., Whitney, S. & Yellowlees, D. 2004. Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37:137-53.
20. Lilley, R. Mc. C., Ralph, P. J. & Larkum, A. W. D. 2010. The determination of activity of the enzyme Rubisco in cell extracts of the dinoflagellate alga Symbiodinium sp. by manganese chemiluminescence and its response to short-term thermal stress of the alga. Plant Cell Environ. 33:995-1004.
21. Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H. & van Woesik, R. 2001. Coral bleaching: the winners and the losers. Ecol. Lett. 4:122-31.
22. Magalon, H., Flot, J. F. & Baudry, E. 2007. Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551-8.
23. Mizusawa, N., Yamamoto, Y. & Miyao, S. 2009. Characterization of damage to the D1 protein of photosystem II under photoinhibitory illumination in non-phosphorylated and phosphorylated thylakoid membranes. J. Photochem. Photobiol. B Biol. 48:97-103.
24. Muscatine, L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. In Dubinsky, Z. [Ed.] Ecosystems of the World. Elsevier, New York, pp. 75-88.
25. Sampayo, E. M., Dove, S. & LaJeunesse, T. C. 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol. Ecol. 18:500-19.
26. Sampayo, E. M., Franceschinis, L., Hoegh-Guldberg, O. & Dove, S. 2007. Niche partitioning of symbiotic dinoflagellates. Mol. Ecol. 16:3721-33.
27. Sampayo, E. M., Ridgway, T., Bongaerts, P. & Hoegh-Gulberg, O. 2008. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc. Natl. Acad. Sci. U. S. A. 105:10444-9.
28. Schreiber, U., Schliwa, U. & Bilger, W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10:51-62.
29. Serodio, S., Vieira, S., Cruz, S. & Coelho, H. 2006. Rapid light-response curves of cholorphyll fluroescence in microalgae:relationship to steady-state light curves and non-photochemical quenching in benthic diatom-dominated assemblages. Photosynth. Res. 90:29-43.
30. Sicher, R. C. 1984. Glycolaldehyde inhibition of photosynthetic carbon assimilation by isolated chloroplasts and protoplasts. Adv. Photosynth. Res. 3:413-6.
31. Taiz, L. & Zeiger, E. 2002. Plant Physiology. Sinauer Associates, Sunderland, Massachusetts, 126 pp.
32. Takahashi, S., Nakamura, T., 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 Physiol. 45:251-5.
33. Takahashi, S., Whitney, S. M. & Badger, M. R. 2009. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc. Natl. Acad. Sci. U. S. A. 106:3237-42.
34. Takahashi, S., Whitney, S., Itoh, S., Maruyama, T. & Badger, M. 2008. Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium. Proc. Natl. Acad. Sci. U. S. A. 105:4203-8.
35. 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. Nat. Acad. Sci. U. S. A. 101:13531-35.
36. Ulstrup, K. E., Ralph, P., Larkum, A. & Kuhl, M. 2006. Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar. Biol. 149:1325-35.
37. 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. 19:291-9.
38. 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. U. S. A. 96:8007.
39. Wooldridge, S. A. 2009. A new conceptual model for the warm-water breakdown of the coral-algae endosymbiosis. Mar. Freshw. Res. 60:483-96.
40. Zardoya, R., Costas, E., Lopez-Rodas, V., Garrido-Pertierra, A. & Bautista, J. M. 1995. Revised dinoflagellate phylogeny inferred from molecular analysis of large-subunit ribosomal RNA gene sequences. J. Mol. Evol. 41:637-45.