Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation

Limnology and Oceanography

Volumn 56, Issue 1, 2011, Pages 139-146

  Hill, Ross ^a   Brown, Christopher M ^b   DeZeeuw, Katrina ^b   Campbell, Douglas A ^b   Ralph, Peter J ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b MOUNT ALLISON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BLEACHING; CORAL; DINOFLAGELLATE; INHIBITION; LIGHT INTENSITY; PHOTOSYNTHESIS; PROTEIN; SYMBIONT; SYMBIOSIS; TEMPERATURE EFFECT;

ANTHOZOA; DINOPHYCEAE; POCILLOPORA DAMICORNIS; SCLERACTINIA;

EID: 78651398839     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2011.56.1.0139     Document Type: Article

References (43)

1. ARO, E.-M., I. VIRGIN, AND B. ANDERSSON. 1993. Photoinhibition of photosystem II: Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143: 113-134, doi:10.1016/ 0005-2728(93)90134-2
2. BHAGOOLI, R., AND M. HIDAKA. 2004. Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses. Comp. Biochem. Physiol. A 137: 547-555, doi:10.1016/j.cbpb.2003.11.008
3. BOUCHARD, J. N., D. A. CAMPBELL, AND S. ROY. 2005. Effects of UV-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, and Argentina). J. Phycol. 41: 273-386, doi:10.1111/ j.1529-8817.2005.04126.x
4. BROWN, B. E. 1997. Coral bleaching: Causes and consequences. Coral Reefs 16: 129-138, doi:10.1007/s003380050249
5. BROWN, B. E. I. AMBARSARI, M. E. WARNER, W. K. FITT, R. P. DUNNE, S. W. GIBB, AND D. G. CUMMINGS. 1999. Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: Evidence for photoinhibition and photoprotection. Coral Reefs 18: 99-105, doi:10.1007/s003380050163
6. BROWN, C. M., D. A. CAMPBELL, AND J. E. LAWRENCE. 2007. Res.ource dynamics during infection of Micromonas pusilla by virus MpV-Sp1. Environ. Microbiol. 9: 2720-2727, doi:10.1111/j.1462-2920.2007.01384.x
7. BROWN, C. M., D. A. CAMPBELL, AND J. E. LAWRENCE, J. D. MACKINNON, A. M. COCKSHUTT, T. VILLAREAL, AND D. A. CAMPBELL. 2008. Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Mar. Biol. 154: 413-422, doi:10.1007/s00227-008-0933-z
8. DEMMIG-ADAMS, B., AND W. W. ADAMS, III. 1992. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 599-626, doi:10.1146/annurev.pp.43.060192.003123
9. EDELMAN, M., AND A. K. MATTOO. 2008. D1-protein dynamics in photosystem II: The lingering enigma. Photosynth. Res. 98: 609-620, doi:10.1007/s11120-008- 9342-x
10. ENRÍQUEZ, S., E. R. MENDEZ, AND R. IGLESIAS-PRIETO. 2005. Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50: 1025-1032, doi:10.4319/lo.2005.50.4.1025
11. HILL, R., AND P. J. RALPH. 2006. Photosystem II heterogeneity of in hospite zooxanthellae in scleractinian corals exposed to bleaching conditions. Photochem. Photobiol. 82: 1577-1585.
12. -, AND -. 2008. Impact of bleaching stress on the function of the oxygen evolving complex of zooxanthellae from scleractinian corals. J. Phycol. 44: 299-310, doi:10.1111/ j.1529-8817.2008.00468.x
13. -, K. E. ULSTRUP, AND P. J. RALPH. 2009. Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated and expelled zooxanthellae from scleractinian corals. Bull. Mar. Sci. 85: 223-244.
14. 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
15. -, AND R. J. JONES. 1999. Photoinhibition and photoprotection in symbiotic dinoflagellates from reef building corals. Mar. Ecol. Prog. Ser. 183: 73-86, doi:10.3354/meps183073
16. JONES, R. J., O. HOEGH-GULDBERG, A. W. D. LARKUM, AND U. SCHREIBER. 1998. Temperature-induced bleaching of corals begins with impairment of the CO2 fixation metabolism in zooxanthellae. Plant Cell Environ. 21: 1219-1230, doi:10.1046/j.1365-3040.1998.00345.x
17. KEY, T., A. MCCARTHY, D. A. CAMPBELL, C. SIX, S. ROY, AND Z. V. FINKEL. 2010. Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ. Microbiol. 12: 95-104, doi:10.1111/j.1462-2920.2009. 02046.x
18. LESSER, M. P., AND J. H. FARRELL. 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
19. MARCUS, Y., H. ALTMAN-GUETA, A. FINKLER, AND M. GUREVITZ. 2003. Dual role of cysteine 172 in redox regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity and degradation. J. Bacteriol. 185: 1509-1517, doi:10.1128/JB.185.5.1509-1517.2003
20. MATTOO, A. K., H. HOFFMAN-FALK, J. B. MARDER, AND M. EDELMAN. 1984. Regulation of protein metabolism: Coupling of photosynthetic electron transport in vivo degradation of the rapidly metabolised 32-kilodalton protein of the chloroplast membranes. Proc. Natl. Acad. Sci. USA 81: 1380-1384, doi:10.1073/pnas.81.5.1380
21. MURATA, N., S. TAKAHASHI, Y. NISHIYAMA, AND S. I. ALLAKHVERDIEV. 2007. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta 1767: 1414-1421.
22. NAKANO, R., H. ISHIDA, A. MAKINO, AND T. MAE. 2006. In vivo fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species in an intact leaf of cucumber under chilling-light conditions. Plant Cell Physiol. 47: 270-276, doi:10.1093/pcp/pci245
23. NISHIYAMA, Y., S. I. ALLAKHVERDIEV, AND N. MURATA. 2005. Inhibition of the repair of PSII by oxidative stress in cyanobacteria. Photosynth. Res. 84: 1-7, doi:10.1007/s11120-004-6434-0
24. -, -, AND -. 2006. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 1757: 742-749, doi:10.1016/j.bbabio.2006.05.013
25. NIXON, P. J., M. BARKER, M. BOEHM, R. DE VRIES, AND J. KOMENDA. 2004. FtsH-mediated repair of the photosystem II complex in response to light stress. J. Exp. Bot. 56: 357-363, doi:10.1093/jxb/eri021
26. -, F. MICHOUX, J. YU, M. BOEHM, AND J. KOMENDA. 2010. Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 106: 1-16, doi:10.1093/aob/mcq059
27. PETROU, K., R. HILL, C. M. BROWN, D. A. CAMPBELL, M. A. DOBLIN, AND P. J. RALPH. 2010. Rapid photoprotection in seaice diatoms from the East Antarctic pack ice. Limnol. Oceanogr. 55: 1400-1407, doi:10.4319/lo.2010.55.3.1400
28. REYNOLDS, J. M., B. U. BRUNS, W. K. FITT, AND G. W. SCHMIDT. 2008. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc. Natl. Acad. Sci. USA 105: 13674-13678, doi:10.1073/pnas.0805187105
29. ROBISON, J. D., AND M. E. WARNER. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42: 568-579, doi:10.1111/j.1529-8817.2006.00232.x
30. SAMPAYO, E. S., L. FRANCESCHINIS, O. HOEGH-GULDBERG, AND S. DOVE. 2007. Niche partitioning of closely related symbiotic dinoflagellates. Mol. Ecol. 16: 3721-3733, doi:10.1111/j.1365-294X.2007.03403.x
31. SARVIKAS, P., M. HAKALA, E. PATSIKKA, T. TYYSTJÄRVI, AND E. TYYSTJÄRVI. 2006. Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol. 47: 391-400, doi:10.1093/pcp/pcj006
32. SILVA, P., AND OTHERS. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. Plant Cell 15: 2152-2164, doi:10.1105/tpc.012609
33. SINCLAIR, J., Y. I. PARK, W. S. CHOW, AND J. M. ANDERSON. 1996. Target theory and the photoinactivation of Photosystem II. Photosynth. Res. 50: 33-40, doi:10.1007/BF00018219
34. SINGLETON, P., AND D. SAINSBURY. 1994. Dictionary of microbiology and molecular biology, 2nd ed. Wiley.
35. SIX, C., Z. V. FINKEL, A. J. IRWIN, AND D. A. CAMPBELL. 2007. Light variability illuminates niche-partitioning among marine picocyanobacteria. PLoS One 12: e1341, doi:10.1371/journal. pone.0001341
36. -, R. SHERRARD, M. LIONARD, S. ROY, AND D. A. CAMPBELL. 2009. Photosystem II and pigment dynamics among ecotypes of the green alga Ostreococcus. Plant Physiol. 151: 379-390, doi:10.1104/pp.109.140566
37. TAKAHASHI, S., S. M. WHITNEY, AND M. R. BADGER. 2009. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc. Natl. Acad. Sci. USA 106: 3237-3242, doi:10.1073/pnas.0808363106
38. -, -, I. SHIGERU, T. MARUYAMA, AND M. R. BADGER. 2008. Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium. Proc. Natl. Acad. Sci. USA 105: 4203-4208, doi:10.1073/pnas.0708554105
39. TYYSTJÄRVI, E. 2008. Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coordin. Chem. Rev. 252: 361-376, doi:10.1016/j.ccr. 2007.08.021
40. ULSTRUP, K. E., R. BERKELMANS, P. J. RALPH, AND M. J. H. VAN OPPEN. 2006. Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: The role of zooxanthellae. Mar. Ecol. Prog. Ser. 314: 135-148, doi:10.3354/meps314135
41. WARNER, M. E., W. K. FITT, AND G. W. SCHMIDT. 1996. The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of coral reef: A novel approach. Plant Cell Environ. 19: 291-299, doi:10.1111/j.1365-3040.1996.tb00251.x
42. -,-, AND-. 1999. Damage to photosystem II in symbioticdinoflagellates: A determinant of coral bleaching. Proc.Natl. Acad. Sci. USA96: 8007-8012, doi:10.1073/pnas.96.14.8007
43. WILSON, M. I., AND OTHERS. 1995. In vivo photomodification of ribulose-1,5-bisphosphate carboxylase/oxygenase holoenzyme by ultraviolet-B radiation. Plant Physiol. 109: 221-229.