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The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis

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Abstract

The mechanism of calcification and its relation to photosynthesis and respiration were studied with Ca2+, pH and O2 microsensors using the scleractinian coral Galaxea fascicularis. Gross photosynthesis (Pg), net photosynthesis (Pn) and dark respiration (DR) were measured on the surface of the coral. Light respiration (LR) was calculated from the difference between Pg and Pn. Pg was about seven times higher than Pn; thus, respiration consumes most of the O2 produced by the algal symbiont's photosynthesis. The respiration rate in light was ca. 12 times higher than in the dark. The coupled Pg and LR caused an intense internal carbon and O2 cycling. The resultant product of this cycle is metabolic energy (ATP). The measured ATP content was about 35% higher in light-incubated colonies than in dark-incubated ones. Direct measurements of Ca2+ and pH were made on the outer surface of the polyp, inside its coelenteron and under the calicoblastic layer. The effects on Ca2+ and pH dynamics of switching on and off the light were followed in these three compartments. Ca2+ concentrations decreased in light on the surface of the polyp and in the coelenteron. They increased when the light was switched off. The opposite effect was observed under the calicoblastic layer. In light, the level of Ca2+ was lower on the polyp surface than in the surrounding seawater, and even lower inside the coelenteron. The concentration of calcium under the calicoblastic layer was about 0.6 mM higher than in the surrounding seawater. Thus Ca2+ can diffuse from seawater to the coelenteron, but metabolic energy is needed for its transport across the calicoblastic layer to the skeleton. The pH under the calicoblastic layer was more alkaline compared with the polyp surface and inside the coelenteron. This rise in pH increased the supersaturation of aragonite from 3.2 in the dark to 25 in the light, and brought about more rapid precipitation of CaCO3. When ruthenium red was added, Ca2+ and pH dynamics were inhibited under the calicoblastic layer. Ruthenium red is a specific inhibitor of Ca-ATPase. The results indicated that Ca-ATPase transports Ca2+ across the calicoblastic layer to the skeleton in exchange for H+. Addition of dichlorophenyldimethylurea completely inhibited photosynthesis. The calcium dynamics under the calicoblastic layer continued; however, the process was less regular. Initial rates were maintained. We conclude that light and not energy generation triggers calcium uptake; however, energy is also needed.

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References

  • Allemand D, Tambutte E, Girard JP, Jaubert J (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin. J Exp Biol 201:2001–2009

    CAS  PubMed  Google Scholar 

  • Barnes DJ (1970) Coral skeletons: an explanation of their growth and structure. Science 170:1305–1308

    CAS  Google Scholar 

  • Barnes DJ, Chalker BE (1990) Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky Z (ed) Ecosystems of the world, coral reefs, vol 25. Elsevier, Amsterdam pp 109–131

  • Benazet-Tambutte S, Allemand D, Jaubert J (1996) Permeability of the oral epithelial layers in cnidarians. Mar Biol 126:43–53

    CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Carlon DB (1996) Calcification rates in corals. Science 274:117

    Article  CAS  Google Scholar 

  • Chalker BE, Taylor DL (1975) Light-enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis. Proc R Soc Lond B Biol Sci 190:323–331

    CAS  PubMed  Google Scholar 

  • Constantz B, Weiner S (1988) Acidic macromolecules associated with mineral phase of scleractinian coral skeletons. J Exp Zool 248:253–258

    CAS  Google Scholar 

  • de Beer D, Schramm A, Santegoeds C, Kühl M (1997) A nitrite microsensor for profiling environmental biofilms. Appl Environ Microbiol Mar 63:973–977

    Google Scholar 

  • de Beer D, Kühl M, Stambler N, 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

    Google Scholar 

  • Fang LS, Chen YWJ, Chen CS (1989) Why does the white tip of stony coral grow so fast without zooxanthellae? Mar Biol 103:359–363

    Google Scholar 

  • Furbank RT, Horton P (1987) Regulation of photosynthesis in isolated barely protoplasts: the contribution of cyclic photophosphorylation. Biochem Biophys Acta 894:332–338

    CAS  Google Scholar 

  • Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457

    CAS  PubMed  Google Scholar 

  • Gattuso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interaction and control by carbonate chemistry. Am Zool 39:160–183

    CAS  Google Scholar 

  • Gattuso JP, Reynaud-Vaganay S, Furla P, Romaine-Lioud S, Jaubert J, Bourge I, Frankignoulle M (2000) Calcification does not stimulate photosynthesis in the zooxanthellate scleractinian coral Stylophora pistillata. Limnol Oceanogr 45:246–250

    Google Scholar 

  • Goreau TF (1959) The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biol Bull (Woods Hole) 116:59–75

    Google Scholar 

  • Goreau TF (1963) Calcium carbonate deposition by coralline algae and corals in relation to their roles as reef-builders. Ann NY Acad Sci 109:127–167

    CAS  Google Scholar 

  • Goreau TJ, Goreau NI, Trench RK, Hayes RL (1996) Calcification rates in corals. Science 271:117

    Google Scholar 

  • Herzig R, Dubinsky Z (1993) Effect of photoacclimation on the energy partitioning between cyclic and non-cyclic photophosphorylation. New Phytol 123:665–672

    CAS  Google Scholar 

  • Ip YK, Lim ALL, Lim RWL (1991) Some properties of calcium-activated adenosine triphosphatase from the hermatypic coral Galaxea fascicularis. Mar Biol 111:191–197

    CAS  Google Scholar 

  • Isa Y, Okazaki M (1987) Some observations on the calcium binding phospholipid from scleractinian coral skeletons. Comp Biochem Physiol B 87:507–512

    Google Scholar 

  • Kingsley RJ, Watabe N (1985) Ca-ATPase localization and inhibition in the gorgonian Leptogorgia virgulata (Lamarck) (Coelentrata: Gorgonacea). J Exp Mar Biol Ecol 93:157–167

    CAS  Google Scholar 

  • Kühl M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172

    Google Scholar 

  • Lucas JM, Knapp LW (1997) A physiological evaluation of carbon sources for calcification in the octocoral Leptogorgia virgulata (Lamarck). J Exp Biol 200:2653–2662

    PubMed  Google Scholar 

  • Marshall AT (1996) Calcification in hermatypic and ahermatypic corals. Science 271:637–639

    CAS  Google Scholar 

  • Marubini F, Thake B (1999) Bicarbonate addition promotes coral growth. Limnol Oceanogr 44:716–720

    CAS  Google Scholar 

  • Marx JL (1973) Photorespiration: key to increasing plant productivity? Science 179:365–367

    Google Scholar 

  • McCloskey LR, Muscatine L (1984) Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proc R Soc Lond B Biol Sci 222:215–230

    Google Scholar 

  • McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth-Sci Rev 42:95–117

    Article  CAS  Google Scholar 

  • Mitterer RM (1978) Amino acid composition and metal binding capability of the skeletal protein of corals. Bull Mar Sci 28:173–180

    CAS  Google Scholar 

  • Pearse VB, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull (Woods Hole) 141:350–363

    Google Scholar 

  • Porter JW, Muscatine L, Dubinsky Z, Falkowski PG (1984) Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proc R Soc Lond B Biol Sci 222:161–180

    Google Scholar 

  • Raven JA (1976) The rate of cyclic and non-cyclic photophosphorylation and oxidative phosphorylation, and regulation of the rate of ATP consumption in Hydrodictyon africanum. New Phytol 76:205–212

    CAS  Google Scholar 

  • Revsbech NP, Jørgensen BB (1983) Photosynthesis of benthic microflora measured with high spatial resolution by the oxygen microprofile method. Limnol Oceanogr 28:749–756

    Google Scholar 

  • Streamer M, McNeil YR, Yellowlees D (1993) Photosynthetic carbon dioxide fixation in zooxanthellae. Mar Biol 115:195–198

    CAS  Google Scholar 

  • Stumm W, Morgan JJ (1996) Aquatic chemistry. Wiley, New York

  • Suzuki A, Nakamori T, Kayanne H (1995) The mechanism of production enhancement on coral reef carbonate systems: model and empirical results. Sediment Geol 99:259–280

    Article  CAS  Google Scholar 

  • Tambutte E, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041

    CAS  PubMed  Google Scholar 

  • Walker D (1992) Excited leaves. New Phytol 121:325–345

    CAS  Google Scholar 

  • Watson EL, Vincenzi FF, Davis PW (1971) Ca2+-activated membrane ATPase: selective inhibition by ruthenium red. Biochim Biophys Acta 249:606–610

    CAS  PubMed  Google Scholar 

  • Yamashiro H (1995) The effect of HEBP, an inhibitor of mineral deposition, upon photosynthesis and calcification in the scleractinian coral, Stylophora pistillata. J Exp Mar Biol Ecol 191:57–63

    Article  CAS  Google Scholar 

  • Young SD, O'Connor JD, Muscatine L (1971) Organic material from scleractinian coral skeletons. II. Incorporation of 14C into protein, chitin and lipid. Comp Biochem Physiol B 40:945–958

    CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the German Federal Ministry of Education and Research (BMBF grants no. 03F0245A). We thank G. Eickert, A. Eggers and I. Schröder for constructing the oxygen electrodes, C. Schönberg, T. Ferdelman, M. Böttcher, C. Stehning, G. Holst and P. Stief for technical support. We also thank the staff of the Marine Science Station in Aqaba, Jordan, for supplying the diving equipment, laboratory space and coral specimens.

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Correspondence to F. A. Al-Horani.

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Communicated by O. Kinne, Oldendorf/Luhe

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Al-Horani, F.A., Al-Moghrabi, S.M. & de Beer, D. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis . Marine Biology 142, 419–426 (2003). https://doi.org/10.1007/s00227-002-0981-8

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  • DOI: https://doi.org/10.1007/s00227-002-0981-8

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