Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Hoogenboom, Mia O ^a,c   Campbell, Douglas A ^b   Beraud, Eric ^a   DeZeeuw, Katrina ^b   Ferrier Pagès, Christine ^a  

^a CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^b MOUNT ALLISON UNIVERSITY   (Canada)

^c JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHLOROPHYLL CONTENT; CONTROLLED STUDY; CORAL REEF; DINOFLAGELLATE; ELECTRON TRANSPORT; FEEDING; FOOD AVAILABILITY; LIGHT; NONHUMAN; PHOTORESPIRATION; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PROTEIN CONTENT; STYLOPHORA PISTILLATA; SYMBIONT; TEMPERATURE STRESS; AEROBIC METABOLISM; ANALYSIS OF VARIANCE; ANIMAL; ANTHOZOA; FOOD; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; RADIATION EXPOSURE; SYMBIOSIS; TEMPERATURE;

ANTHOZOA; COELENTERATA; DINOPHYCEAE; SCLERACTINIA; STYLOPHORA PISTILLATA; TURBINARIA RENIFORMIS;

CHLOROPHYLL;

AEROBIOSIS; ANALYSIS OF VARIANCE; ANIMALS; ANTHOZOA; CHLOROPHYLL; DINOFLAGELLIDA; ELECTRON TRANSPORT; FOOD; LIGHT; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PRINCIPAL COMPONENT ANALYSIS; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TEMPERATURE;

EID: 84855854552     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030167     Document Type: Article

References (63)

1. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933.
2. Baird AH, Bhagooli R, Ralph PJ, Takahashi S, (2009) Coral bleaching: the role of the host. Trends in Ecology and Evolution 24: 16-20.
3. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
4. Wilkinson C, Linden O, Cesar H, Hodgson G, Rubens J, et al. (1999) Ecological and socioeconomic impacts of 1998 coral mortality in the Indian Ocean: An ENSO impact and a warning of future change? Ambio 28: 188-196.
5. Bruno JF, Selig ER, (2007) Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2: e711.
6. Burke L, Reytar K, Spalding M, Perry A, (2011) Reefs at Risk Revisited. Washington World Resources Institute.
7. Hoegh-Guldberg O, (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine & Freshwater Research 50: 839-866.
8. Warner ME, Fitt WK, Schmidt GW, (1999) Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proceedings of the National Academy of Sciences of the United States of America 96: 8007-8012.
9. Takahashi S, Whitney SM, Badger MR, (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proceedings of the National Academy of Sciences of the United States of America 106: 3237-3242.
10. Hill R, Brown CM, DeZeeuw K, Campbell DA, Ralph PJ, (2011) Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation. Limnology & Oceanography 56: 139-146.
11. Leggat W, Whitney S, Yellowlees D, (2004) Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37: 137-153.
12. Lilley RM, Ralph P, Larkum A, (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 & Environment 33: 995-1004.
13. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U, (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell & Environment 21: 1219-1221.
14. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA, (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Marine Ecology Progress Series 272: 117-130.
15. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, et al. (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Science, USA 101: 13531-13535.
16. 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. Proceedings of the National Academy of Sciences of the United States of America 105: 4203-4208.
17. Maxwell K, Johnson GN, (2000) Chlorophyll fluorescence- a practical guide. Journal of Experimental Botany 51: 659-668.
18. Schreiber U, Bilger W, Neubauer C, (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM, editors. Ecophysiology of Photosynthesis Berlin Springer-Verlag pp. 49-70.
19. Brown BE, Dunne RP, Warner ME, Ambarsari I, Fitt WK, et al. (2000) Damage and recovery of Photosystem II during a manipulative field experiment on solar bleaching in the coral Goniastrea aspera. Marine Ecology-Progress Series 195: 117-124.
20. Winters G, Loya Y, Roettgers R, Beer S, (2003) Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnology & Oceanography 48: 1388-1393.
21. Lesser MP, Gorbunov MY, (2001) Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Marine Ecology-Progress Series 212: 69-77.
22. Hill R, Ralph PJ, (2008) Impact of bleaching stress on the function of the oxygen evolving complex of zooxanthellae from scleractinian corals. Journal of Phycology 44: 299-310.
23. Klughammer C, Schreiber U, (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Application Notes 1: 11-14.
24. Lesser MP, Farrell JH, (2004) Solar radiation increases the damage to both host tissues and algal symbionts of corals exposed to thermal stress. Coral Reefs 23: 367-377.
25. Stimson J, Kinzie R, (1991) The diel pattern of release of zooxanthellae by colonies of Pocillopora damicornis maintained under control and nitrogen-enriched conditions. Journal of Experimental Marine Biology & Ecology 153: 63-74.
26. Hughes AD, Grottoli AG, Pease TK, Matsui Y, (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Marine Ecology-Progress Series 420: 91-101.
27. Grottoli AG, Rodrigues LJ, Palardy JE, (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440: 1186-1189.
28. Palardy JE, Rodrigues LJ, Grottoli AG, (2008) The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. Journal of Experimental Marine Biology and Ecology 367: 180-188.
29. Davies PS, (1991) Effect of daylight variations on the energy budgets of shallow-water corals. Marine Biology 108: 137-144.
30. Jeffery SW, Humphrey GF, (1975) New spectrophotometric equations for determining chlorophylls a, b, c and c2 in higher plants, algae and natural phytoplankton. Biochimica et Biophysica Acta 167: 191-194.
31. Campbell DA, Cockshutt AM, Porankiewicz-Asplundb J, (2003) Analysing photosynthetic complexes in uncharacterized species or mixed microalgal communities using global antibodies. Physiologia Plantarum 119: 322-327.
32. Brown CM, MacKinnon JD, Cockshutt AM, Villareal TA, Campbell DA, (2008) Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Marine Biology 151.
33. Fitt WK, Brown BE, Warner ME, Dunne RP, (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20: 51-65.
34. Bhagooli R, Hidaka M, (2004) Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata in response to thermal and light stresses. Comparative Biochemistry and Physiology A- Molecular & Integrative Physiology 137: 547-555.
35. Borell EM, Yuliantri AR, Bischof K, Richter C, (2008) The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. Journal of Experimental Marine Biology and Ecology 364: 116-123.
36. Ferrier-Pages C, Hoogenboom MO, Houlbreque F, (2011) The Role of Plankton in Coral Trophodynamics. In: Dubinsky Z, Stambler N, editors. Coral reefs: An ecosystem in transition Springer pp. 215-229.
37. Treignier C, Grover R, Ferrier-Pages C, (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnology & Oceanography 53: 2702-2710.
38. Ferrier-Pages C, Rottier C, Beraud E, Levy O, (2010) Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: Effect on the rates of photosynthesis. Journal of Experimental Marine Biology and Ecology 390: 118-124.
39. Bouchard JN, Longhi ML, Roy S, Campbell DA, Ferreyra G, (2008) Interaction of nitrogen status and UVB sensitivity in a temperate phytoplankton assemblage. Journal of Experimental Marine Biology & Ecology 359: 67-76.
40. Pompelli MF, Martins SCV, Antunes WC, Chaves ARM, DaMatta FM, (2010) Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. Journal of Plant Physiology 167: 1052-1060.
41. Umena Y, Kawakami K, Shen J-R, Kamiya N, (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9A. Nature 473: 55-61.
42. Ben-Shem A, Frolow F, Nelson N, (2003) Crystal structure of plant photosystem I. Nature 426: 630-635.
43. Iglesias-Prieto R, Trench RK, (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Marine Biology 130: 23-33.
44. Falkowski PG, Raven JA, (2007) Aquatic photosynthesis. New Jersey Princeton University Press.
45. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ, (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28: 179-195.
46. Ferrier-Pages C, Richard C, Forcioli D, Allemand D, Pichon M, et al. (2007) Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species. Biological Bulletin 213: 76-87.
47. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W, (2008) A community change in the algal endosymbionts in a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B-Biological Sciences 275: 1359-1365.
48. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM, (2008) In situ photobiology of corals over large depth ranges: A multivariate analysis on the roles of environment, host, and algal symbiont. Limnology & Oceanography 53: 2711-2723.
49. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW, (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proceedings of the National Academy of Science, USA 105: 13674-13678.
50. Bruce D, Vasil'ev S, (2004) Excess light stress: multiple dissipative processes of excess excitation. In: Papageorgiou GC, Govindjee, editors. Chlorophyll a fluorescence: A signature of photosynthesis Amsterdam Springer pp. 497-523.
51. Gorbunov MY, Kolber ZS, Lesser MP, Falkowski PG, (2001) Photosynthesis and photoprotection in symbiotic corals. Limnology & Oceanography 46: 75-85.
52. Hoegh-Guldberg O, Jones RJ, (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Marine Ecology Progress Series 183: 73-86.
53. Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV, (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408: 613-615.
54. Allen JF, (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends in Plant Science 8: 15-19.
55. Munekage Y, Hashimoto M, Miyake C, Tomizawa K-I, Endo T, et al. (2004) Cyclic electron flow around photosystem 1 is essential for photosynthesis. Nature 429: 581-582.
56. Heber U, Walker D, (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiology 100: 1621-1626.
57. Johnson GN, (2005) Cyclic electron transport in C3 plants: fact or artefact. Journal of Experimental Biology 55: 407-416.
58. MacKenzie TDB, Johnson JM, Cockshutt AM, Burns RA, Campbell DA, (2005) Large reallocations of carbon, nitrogen, and photosynthetic reductant among phycobilisomes, photosystems, and Rubisco during light acclimation in Synechococcus elongatus strain PCC7942 are constrained in cells under low environmental inorganic carbon. Archives of Microbiology 183: 190-202.
59. Ogawa T, Kaplan A, (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynthesis Research 77: 105-115.
60. Whitney SM, Andrews TJ, (1998) The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae. Australian Journal of Plant Physiology 25: 131-138.
61. Borell EM, Bischof K, (2008) Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157: 593-601.
62. Behrenfeld MJ, Prasil O, Kolber ZS, Babin M, Falkowski PG, (1998) Compensatory changes in Photosystem II electron transport rates protect photosynthesis from photoinhibition. Photosynthesis Research 58: 259-268.
63. Sukenik A, Bennett J, Falkowski P, (1987) Light-saturated photosynthesis- limitation by electron-transport or carbon fixation. Biochimica Et Biophysica Acta 891: 205-215.