The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host

Plant, Cell and Environment

Volumn 26, Issue 12, 2003, Pages 1951-1961

  Leggat, W ^a,b   Buck, B H ^a,c   Grice, A ^a   Yellowlees, D ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

Ammonium; Bleaching; Carbonic anhydrase; Giant clam; Glutamine synthetase; Inorganic carbon; Symbiosis; Zooxanthellae

Indexed keywords

AMMONIUM; BIVALVE; BLEACHING; DINOFLAGELLATE; HOST-SYMBIONT INTERACTION; INORGANIC CARBON; METABOLISM; ZOOXANTHELLA;

BIVALVIA; DINOPHYCEAE; INVERTEBRATA; TRIDACNA; TRIDACNA GIGAS; TRIDACNIDAE;

EID: 0347664166     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.0016-8025.2003.01111.x     Document Type: Article

References (65)

1. Ambariyanto & Hoegh-Guldberg O. (1997) Effect of nutrient enrichment in the field on the biomass, growth and calcification of the giant clam Tridacna maxima. Marine Biology 129, 635-642.
2. Anderson S.L. & Burris J.E. (1987) Role of glutamine synthetase in ammonia assimilation by symbiotic marine dinoflagellates (zooxanthellae). Marine Biology 94, 451-458.
3. Baillie B. & Yellowlees D. (1998) Characterization and function of carbonic anhydrase in the zooxanthellae-giant clam symbiosis. Proceedings of the Royal Society of London, Series B 265, 465-473.
4. Belda C.A., Lucas J.S. & Yellowlees D. (1993) Nutrient limitation in the giant clam-zooxanthellae symbiosis: effects of nutrient supplements on growth of the symbiotic partners. Marine Biology 117, 655-664.
5. Belda-Baillie C.A., Leggat W. & Yellowlees D. (1998) Growth and metabolic responses of the giant clam-zooxanthellae symbiosis in a reef-fertilisation experiment. Marine Ecology Progress Series 170, 131-141.
6. Berkelmans R. & Oliver J.K. (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18, 55-60.
7. Böttcher K., Siebers D., Becker W. & Petrausch G. (1991) Physiological role of branchial carbonic anhydrase in the shore crab Carcinus maenus. Marine Biology 110, 337-342.
8. Bradford M.M. (1976) A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
9. Brown B.E. (1997) Coral bleaching: causes and consequences. Coral Reefs 16, 129-138.
10. Brown B.E. & Suharsono (1990) Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8, 163-170.
11. Brown B.E., Dunne R.P., Warner M.E., Ambarsari I., Fitt W.K., Gibb S.W. & Cummings D.O. (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.
12. Buck B.H., Rosenthal H. & Saint-Paul U. (2002) Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriaticum and Tridacna gigas. Aquatic Living Resources 15, 107-117.
13. Bunkley-Williams L., Morelock J. & Williams E.H.J.R. (1991) Lingering effects of the 1987 mass bleaching of Puerto Rican coral reefs in mid to later 1988. Journal of Aquatic Animal Health 3, 242-247.
14. Dal Pont G., Hogan M. & Newell B. (1974) Laboratory techniques in marine chemistry II Determination of ammonia in seawater and the preservation of samples for nitrate analysis. CSIRO Division of Fisheries and Oceanography Report 55, 1-5.
15. Davy S.K. & Cook C.B. (2001) The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida. Marine Biology 139, 999-1005.
16. Ferrier-Pagès C., Schoelzke V., Jaubert J., Muscatine L. & Hoegh-Guldberg O. (2001) Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrichment. Journal of Experimental Marine Biology and Ecology 259, 249-261.
17. Fisher C.R., Fitt W.K. & Trench R.K. (1985) Photosynthesis and respiration in Tridacna gigas as a function of irradiance and size. Biology Bulletin 169, 230-245.
18. Fitt W.K., Rees T.A.V., Braley R.D., Lucas J.S. & Yellowlees D. (1993) Nitrogen flux in giant clams: size-dependency and relationship to zooxanthellae density and clam biomass in the uptake of dissolved inorganic nitrogen. Marine Biology 117, 381-386.
19. Fitt W.K., Rees T.A.V. & Yellowlees D. (1995) Relationship between pH and the availability of dissolved inorganic nitrogen in the zooxanthellae-giant clam symbiosis. Limnology and Oceanography 40, 976-982.
20. Gates R.D. (1990) Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8, 193-197.
21. Gates R.D., Baghdasarian G. & Muscatine L. (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biology Bulletin 189, 324-332.
22. Geladopoulos T.P., Sotiroudis T.G. & Evangelopoulos A.E. (1991) A malachite green colorimetric assay for protein phosphatase activity. Analytical Biochemistry 192, 112-116.
23. Glynn P.W. (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1-17.
24. Glynn P.W. (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biology 2, 495-509.
25. Harlow E. & Lane D. (1988) Antibodies, a Laboratory Manual. Cold Spring Harbor Laboratory, New York, USA.
26. Henry R.P. (1996) Multiple roles of carbonic anhydrase in cellular transport and metabolism. Annual Review of Physiology 58, 523-538.
27. Hoegh-Guldberg O. (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50, 839-866.
28. Hoegh-Guldberg O. & Smith G.J. (1989a) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. Journal of Experimental Marine Biology and Ecology 129, 279-304.
29. Hoegh-Guldberg O. & Smith G.J. (1989b) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Marine Ecology Progress Series 57, 173-186.
30. Iglesias-Prieto R., Malta J.L., Robins W.A. & Trench R.K. (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proceedings of the National Academy of Science of the USA 89, 10302-10305.
31. Ishikura M., Adachi K. & Maruyama T. (1999) Zooxanthellae release glucose in the tissue of a giant clam, Tridacna crocea. Marine Biology 133, 665-673.
32. Jones R.J. (1997) Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Marine Ecology Progress Series 158, 51-59.
33. 2 fixation mechanism in zooxanthellae. Plant, Cell and Environment 21, 1219-1230.
34. Kushmaro A., Loya Y., Fine M. & Rosenberg E. (1996) Bacterial infection and coral bleaching. Nature 380, 396.
35. Laemmli U.K. (1970) Cleavage of structural proteins during assembly of the head bacteriophage T4. Nature 227, 680-685.
36. Le Tissier M.D.A. & Brown B.E. (1996) Dynamics of solar bleaching in the intertidal reef coral Goniastrea aspera at Ko Phuket, Thailand. Marine Ecology Progress Series 136, 235-244.
37. Leder J.J., Szmant A.M. & Swart P.K. (1991) The effect of prolonged 'bleaching' on skeletal banding and stable isotopic composition in Montastrea annularis: preliminary observations. Coral Reefs 10, 19-27.
38. Leggat W., Badger M.R. & Yellowlees D. (1999) Evidence for an inorganic carbon concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiology 121, 1247-1255.
39. Leggat W., Marendy E., Baillie B., Whitney S.M., Ludwig M., Badger M.R. & Yellowlees D. (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition of inorganic carbon. Functional Plant Biology 29, 309-322.
40. 2 by symbionts in the giant clam Tridacna gigas. Proceedings of the Royal Society of London B 267, 523-529.
41. Lesser M.P. & Shick J.M. (1989) Effects of irradiance and ultraviolet radiation in photoadaption in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defences against oxygen toxicity. Marine Biology 102, 243-255.
42. 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 oxygen radicals. Coral Reefs 8, 225-232.
43. Lesser M.P., Weis V.M. & Patterson M.R. & Jokiel P.L. (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): Diffusion barriers, inorganic carbon limitation, and biochemical plasticity. Journal of Experimental Marine Biology and Ecology 178, 153-179.
44. Miller D.J. & Yellowlees D. (1989) Inorganic nitrogen uptake by symbiotic: marine cnidarians: a critical review. Proceedings of the Royal Society of London Series B 237, 109-125.
45. Mumby P.J., Chisholm J.R.M., Edwards A.J., Clark C.D., Roark E.B., Andrefouet S. & Jaubert J. (2001) Unprecedented bleaching-induced mortality in Parites spp. at Rogiroa Atoll, French Polynesia. Marine Biology 139, 183-189.
46. Muscatine L. & D'Elia C.F. (1978) The uptake, retention, and release of ammonia by reef corals. Limnology and Oceanography 23, 725-734.
47. Norton J.H., Prior H.C., Baillie B. & Yellowlees D. (1995) Atrophy of the zooxanthellal tubular system in bleached giant clams Tridacna gigas. Journal of Invertebrate Pathology 66, 307-310.
48. Rees T.A.V., Fitt W.K., Baillie B. & Yellowlees D. (1993b) A method for temporal measurement of haemolymph composition in the giant clam symbiosis and its application to glucose and glycerol levels during a diel cycle. Limnology and Oceanography 38, 213-217.
49. Rees T.A.V., Fitt W.K. & Yellowlees D. (1993a) The haemolymph and its temporal relationship with zooxanthellae metabolism in the giant clam symbiosis. In Biology and Mariculture of Giant Clams. (ed. W.K. Fitt) ACIAR Proceedings 47, pp. 41-44. Pirie Printers, Canberra, Australia.
50. Rees T.A.V., Fitt W.K. & Yellowlees D. (1994) Host glutamine synthetase activities in the giant clam-zooxanthellae symbiosis: effects of clam size, elevated ammonia and continuous darkness. Marine Biology 118, 681-685.
51. Rees T.A.V., Larson T.R., Heldens J.W.G. & Huning F.G.J. (1995) In situ glutamine synthetase activity in a marine unicellular alga: development of a sensitive colorimetric assay and the effects of nitrogen status on enzyme activity. Plant Physiology 104, 1405-1410.
52. Shepherd D., Leggat W., Rees T.A.V. & Yellowlees D. (1999) Ammonium, but not nitrate, stimulates an increase in glutamine concentration in the haemolymph of Tridacna gigas. Marine Biology 133, 45-53.
53. StatSoft Inc (1995) STATISTICA for Windows [Computer Program Manual]. StatSoft Inc., Tulsa, OK, USA.
54. Streamer M., Griffiths D.J. & Thinh L. (1988) The products of photosynthesis by zooxanthellae (Symbiodinium microadriaticum) of Tridacna gigas and their transfer to the host. Symbiosis 6, 237-252.
55. Swanson R. & Hoegh-Guldberg O. (1998) Amino acid synthesis in the symbiotic sea anemone Aiptasia pulchella. Marine Biology 131, 83-93.
56. Szmant A.M. & Gassman N.J. (1990) The effects of prolonged 'bleaching', on tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8, 217-224.
57. Vicente V.P. (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8, 199-202.
58. Wang J.T. & Douglas A.E. (1998) Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis. Journal of Experimental Biology 201, 2445-2453.
59. Warner M.E., Fitt W.K. & Schmidt G.W. (1996) The effects of elevated temperature in the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant, Cell and Environment 19, 291-299.
60. Weis V.M. (1991) The induction of carbonic anhydrase in the symbiotic sea anemone Aiptasia pulchella. Biology Bulletin 180, 496-504.
61. Weis V.M. & Levine R.P. (1996) Differential protein profiles reflect the different lifestyles of symbiotic and aposymbiotic Anthopleura elegantissma, a sea anemone from temperate waters. Journal of Experimental Biology 199, 883-892.
62. Weis V.M. & Reynolds W.S. (1999) Carbonic anhydrase expression and synthesis in the sea anemone Anthopleura elegantissma are enhances by the presence of dinoflagellate symbionts. Physiological and Biochemical Zoology 72, 307-316.
63. Wilkerson P.P. & Muscatine L. (1984) Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic anemone (Aiptasia pulchella). Proceedings of the Royal Society of London B 221, 71-86.
64. van Woesik R., De Vantier L.M. & Glazebrook J.S. (1995) Effects of cyclone 'Joy' on nearshore coral communities of the Great Barrier Reef. Marine Ecology Progress Series 128, 261-270.
65. Yellowlees D., Dionisio-Sese M.L., Masuda K., Maruyama T., Abe T., Baillie B., Tsuzuki M. & Miyachi S. (1993) Role of carbonic anhydrase in the supply of inorganic carbon to the giant clamzooxanthellae symbiosis. Marine Biology 115, 605-611.