The influence of photosynthesis on host intracellular ph in scleractinian corals

Journal of Experimental Biology

Volumn 216, Issue 8, 2013, Pages 1398-1404

  Laurent, Julien ^a   Tambutté, Sylvie ^a   Tambutté, Éric ^a   Allemand, Denis ^a   Venn, Alexander ^a  

^a CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

Author keywords

Acid base balance; Cnidarian; Irradiance; Stylophora pistillata; Symbiosis

Indexed keywords

ANIMAL; ANTHOZOA; ARTICLE; DINOFLAGELLATE; LIGHT; PH; PHOTOSYNTHESIS; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; ANTHOZOA; DINOFLAGELLIDA; HYDROGEN-ION CONCENTRATION; LIGHT; PHOTOSYNTHESIS; SYMBIOSIS;

ANIMALIA; ANTHOZOA; CNIDARIA; DINOPHYCEAE; SCLERACTINIA; STYLOPHORA PISTILLATA;

EID: 84875133733     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.082081     Document Type: Article

References (50)

1. Al-Horani, F. A., Al-Moghrabi, S. M. and de Beer, D. (2003). The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar. Biol. 142, 419-426.
2. Al-Moghrabi, S., Goiran, C., Allemand, D., Speziale, N. and Jaubert, J. (1996). Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association II. Mechanisms for bicarbonate uptake. J. Exp. Mar. Biol. Ecol. 199, 227-248.
3. Allemand, D., Furla, P. and Bénazet-Tambutté, S. (1998). Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can. J. Bot. 76, 925-941.
4. Allemand, D., Ferrier-Pagès, C., Furla, P., Houlbrèque, F., Puverel, S., Reynaud, S., Tambutté, É., Tambutté, S. and Zoccola, D. (2004). Biomineralisation in reefbuilding corals: From molecular mechanisms to environmental control. C. R. Palevol. 3, 453-467.
5. Anthony, K. R., Kline, D. I., Diaz-Pulido, G., Dove, S. and Hoegh-Guldberg, O. (2008). Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl. Acad. Sci. USA 105, 17442-17446.
6. Bonar, P. T. and Casey, J. R. (2008). Plasma membrane Cl-/HCO3 - exchangers: Structure, mechanism and physiology. Channels 2, 337-345.
7. Boron, W. F. (2004). Regulation of intracellular pH. Adv. Physiol. Educ. 28, 160-179.
8. Boussouf, A. and Gaillard, S. (2000). Intracellular pH changes during oligodendrocyte differentiation in primary culture. J. Neurosci. Res. 59, 731-739.
9. Brownlee, C. (2009). pH regulation in symbiotic anemones and corals: A delicate balancing act. Proc. Natl. Acad. Sci. USA 106, 16541-16542.
10. Busa, W. B. (1986). Mechanisms and consequences of pH-mediated cell regulation. Annu. Rev. Physiol. 48, 389-402.
11. Busa, W. B. and Nuccitelli, R. (1984). Metabolic regulation via intracellular pH. Am. J. Physiol. 246, R409-R438.
12. Casey, J. R., Grinstein, S. and Orlowski, J. (2010). Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11, 50-61.
13. Crawley, A., Kline, D. I., Dunn, S., Anthony, K. E. N. and Dove, S. (2010). The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob. Change Biol. 16, 851-863.
14. de Beer, D., Kühl, M., Stambler, N. and Vaki, L. (2000). A microsensor study of light enhanced Ca2+ uptake and photosynthesis in the reef-building hermatypic coral Favia sp. Mar. Ecol. Prog. Ser. 194, 75-85.
15. Denker, S. P., Huang, D. C., Orlowski, J., Furthmayr, H. and Barber, D. L. (2000). Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H+ translocation. Mol. Cell 6, 1425-1436.
16. Dubbin, P. N., Cody, S. H. and Williams, D. A. (1993). Intracellular pH mapping with SNARF-1 and confocal microscopy. II: PH gradients within single cultured cells. Micron 24, 581-586.
17. Ferrier-Pagès, C., Gattuso, J. P., Dallot, S. and Jaubert, J. (2000). Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19, 103-113.
18. Fitt, W. K. (2000). Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. Biol. Bull. 198, 110-120.
19. Frank, H. A. and Cogdell, R. J. (1996). Carotenoids in photosynthesis. Photochem. Photobiol. 63, 257-264.
20. Furla, P., Galgani, I., Durand, I. and Allemand, D. (2000). Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J. Exp. Biol. 203, 3445-3457.
21. Garrigue, C., Clavier, J. and Boucher, G. (1992). The use of photosynthesis inhibitor (DCMU) for in situ metabolic and primary production studies on soft bottom benthos. Hydrobiologia 246, 141-145.
22. Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50, 839-866.
23. Hoegh-Guldberg, O., Mumby, P.-J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K. et al. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742.
24. Jeffrey, S. W. and Humphrey, G. F. (1975). New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191-194.
25. Jokiel, P. L. (2011). Ocean acidification and control of reef coral calcification by boundary layer limitation of proton flux. Bull. Mar. Sci. 87, 639-657.
26. Jones, R. J. (2004). Testing the ?photoinhibition' model of coral bleaching using chemical inhibitors. Mar. Ecol. Prog. Ser. 284, 133-145.
27. Kazandjian, A., Shepherd, V. A., Rodriguez-Lanetty, M., Nordemeier, W., Larkum, A. W. D. and Quinnell, R. G. (2008). Isolation of symbiosomes and the symbiosome membrane complex from the zoanthid Zoanthus robustus. Phycologia 47, 294-306.
28. Kühl, M., Cohen, Y., Dalsgaard, T., Jorgensen, B. B. and Revsbech, N. P. (1995). Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Prog. Ser. 117, 159-172.
29. Kurkdjian, A. and Guern, J. (1989). Intracellular pH: Measurement and importance in cell activity. Annu. Rev. Plant Physiol. 40, 271-303.
30. Lemasters, J. J., Trollinger, D. R., Qian, T., Cascio, W. E. and Ohata, H. (1999). Confocal imaging of Ca2+, pH, electrical potential, and membrane permeability in single living cells. Methods Enzymol. 302, 341-358.
31. Lesser, M. P. (2007). Coral reef bleaching and global climate change: Can corals survive the next century? Proc. Natl. Acad. Sci. USA 104, 5259-5260.
32. Levy, O., Achituv, Y., Yacobi, Y. Z., Dubinsky, Z. and Stambler, N. (2006). Diel ?tuning' of coral metabolism: Physiological responses to light cues. J. Exp. Biol. 209, 273-283.
33. Levy, O., Kaniewska, P., Alon, S., Eisenberg, E., Karako-Lampert, S., Bay, L. K., Reef, R., Rodriguez-Lanetty, M., Miller, D. J. and Hoegh-Guldberg, O. (2011). Complex diel cycles of gene expression in coral-algal symbiosis. Science 331, 175.
34. Madshus, I. H. (1988). Regulation of intracellular pH in eukaryotic cells. Biochem. J. 250, 1-8.
35. Muscatine, L. (1990). The role of symbiotic algae in carbon and energy flux in reef corals. In Coral Reefs (ed. Z. Dubinsky), pp. 75-84. Amsterdam: Elsevier.
36. Putney, L. K. and Barber, D. L. (2003). Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition. J. Biol. Chem. 278, 44645-44649.
37. Raven, J. A. and Smith, F. A. (1980). Intracellular pH regulation in the giant-celled marine alga Chaetomorpha darwinii. J. Exp. Bot. 31, 1357-1369.
38. Romaine, S., Tambutté, E., Allemand, D. and Gattuso, J. P. (1997). Photosynthesis, respiration and calcification of a zooxanthellate scleractinian coral under submerged and exposed conditions. Mar. Biol. 129, 175-182.
39. Roos, A. and Boron, W. F. (1981). Intracellular pH. Physiol. Rev. 61, 296-434.
40. Russell, J. M. and Boron, W. F. (1976). Role of choloride transport in regulation of intracellular pH. Nature 264, 73-74.
41. Smith, F. A. and Raven, J. A. (1979). Intracellular pH and its regulation. Annu. Rev. Plant Physiol. 30, 289-311.
42. Tambutté, S., Holcomb, M., Ferrier-Pagès, C., Reynaud, S., Tambutté, É., Zoccola, D. and Allemand, D. (2011). Coral biomineralization: From the gene to the environment. J. Exp. Mar. Biol. Ecol. 408, 58-78.
43. Trench, R. K. (1993). Microalgal-invertebrate symbioses: A review. Endocytobiosis Cell Res. 9, 135-176.
44. Venn, A. A., Loram, J. E. and Douglas, A. E. (2008). Photosynthetic symbioses in animals. J. Exp. Bot. 59, 1069-1080.
45. Venn, A. A., Tambutté, E., Lotto, S., Zoccola, D., Allemand, D. and Tambutté, S. (2009). Imaging intracellular pH in a reef coral and symbiotic anemone. Proc. Natl. Acad. Sci. USA 106, 16574-16579.
46. Venn, A. A., Tambutté, E., Holcomb, M., Allemand, D. and Tambutté, S. (2011). Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6, e20013.
47. Weis, V. M. and Allemand, D. (2009). Physiology. What determines coral health? Science 324, 1153-1155.
48. Weis, V. M., Davy, S. K., Hoegh-Guldberg, O., Rodriguez-Lanetty, M. and Pringle, J. R. (2008). Cell biology in model systems as the key to understanding corals. Trends Ecol. Evol. 23, 369-376.
49. Wilkerson, F. P., Muller Parker, G. and Muscatine, L. (1983). Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol. Oceanogr. 28, 1009-1014.
50. Yellowlees, D., Rees, T. A. V. and Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31, 679-694.