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A New Coral Carbonic Anhydrase in Stylophora pistillata

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Abstract

Scleractinian corals are of particular interest due to their ability to establish an intracellular mutualistic symbiosis with phototrophic dinoflagellates and to deposit high rates of calcium carbonate in their skeleton. Carbonic anhydrases have been shown to play a crucial role in both processes. In this study, we report the molecular cloning and characterization of a novel α-CA in the coral Stylophora pistillata. This enzyme shares homologies with the human isoform CA II and is referred to as STPCA-2. STPCA-2 is 35.2 kDa and possesses all key amino acids for catalytic activity. With a ratio between catalytic and Michaelis constants (kcat/Km) of 8.3.107 M−1 s−1 is considered as highly active. Owing to its intracellular localisation in the oral endoderm and in the aboral tissue, we propose that STPCA-2 is involved in pH regulation and/or inorganic carbon delivery to symbiont and calcification.

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References

  • Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Al-Horani FA, Al-Moghrabi SM, de Beer D (2003a) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15

    Article  Google Scholar 

  • Al-Horani FA, Al-Moghrabi SM, de Beer D (2003b) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    CAS  Google Scholar 

  • Al-Moghrabi S, Goiran C, Allemand D, Speziale N, 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

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Innocenti A, Zoccola D, Scozzafava A, Allemand D, Tambutté S, Supuran CT (2009a) Carbonic anhydrase inhibitors: inhibition studies of a coral secretory isoform with inorganic anions. Bioorg Med Chem Lett 19:650–653

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Innocenti A, Zoccola D, Scozzafava A, Tambutté S, Supuran CT (2009b) Carbonic anhydrase inhibitors. Inhibition studies of a coral secretory isoform by sulfonamides. Bioorg Med Chem 17:5054–5058

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Tambutté E, Tambutté S, Allemand D, Zoccola D (2010a) Symbiosis-dependent gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H+-ATPase gene. Proc R Soc B 277:87–95

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Zoccola D, Tambutté S, Vullo D, Supuran CT (2010b) Carbonic anhydrases activators. the first activation study of a coral secretory isoform with amino acids and amines. Bioorg Med Chem 18:2300–2303

    Article  PubMed  CAS  Google Scholar 

  • Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362

    Article  PubMed  CAS  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890

    Article  PubMed  CAS  Google Scholar 

  • deBoer ML, Krupp DA, Weis VM (2006) Two atypical carbonic anhydrase homologs from the planula larva of the scleractinian coral Fungia scutaria. Biol Bull 211:18–30

    Article  PubMed  CAS  Google Scholar 

  • Eisenhaber B, Bork P, Eisenhaber F (1999) Prediction of potential GPI-modification sites in proprotein sequences. J Mol Biol 292:741–758

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971

    Article  PubMed  CAS  Google Scholar 

  • Erez J (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273:199–202

    Article  CAS  Google Scholar 

  • Furla P, Bénazet-Tambutté S, Jaubert J, Allemand D (1998) Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. Am J Physiol 274:R303–R310

    PubMed  CAS  Google Scholar 

  • Furla P, Allemand D, Orsenigo M (2000a) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am J Physiol Regul Integr Comp Physiol 278:R870–R881

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131

    Article  PubMed  CAS  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, Mar Biol Lab, Woods Hole 116:59–75

    Article  CAS  Google Scholar 

  • Grasso L, Maindonald J, Rudd S, Hayward DC, Saint R, Miller DJ, Ball EE (2008) Microarray analysis identities candidate genes for key roles in coral development. BMC Genomics 9:540

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hewett-Emmett D, Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol 5:50–77

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck, Ronquist (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Isa Y, Yamazato K (1984) The distribution of carbonic anhydrase in a staghorn coral Acropora hebes (Dana). Galaxea 3:25–36

    CAS  Google Scholar 

  • Jackson DJ, Macis L, Reitner J, Degnan BM, Worheide G (2007) Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis. Science 316:1893–1895

    Article  PubMed  CAS  Google Scholar 

  • Khalifah RG (1971) The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 246:2561–2573

    PubMed  CAS  Google Scholar 

  • Kingsley RJ, Watabe N (1987) Role of carbonic anhydrase in calcification in the gorgonian Leptogorgia virgulata. J Exp Zool 241:171–180

    Article  CAS  Google Scholar 

  • Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255

    Article  PubMed  CAS  Google Scholar 

  • Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, Badger MR, Yellowlees D (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29:309–322

    Article  CAS  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  CAS  Google Scholar 

  • Marshall AT, Clode PL (2003) Light-regulated Ca2+ uptake and O2 secretion at the surface of a scleractinian coral Galaxea fascicularis. Comp Biochem Physiol A Mol Integr Physiol 136:417–426

    Article  PubMed  Google Scholar 

  • McCall KA, Huang C, Fierke CA (2000) Function and mechanism of zinc metalloenzymes. J Nutr 130:1437S–1446S

    PubMed  CAS  Google Scholar 

  • Miyamoto H, Miyashita T, Okushima M, Nakano S, Morita T, Matsushiro A (1996) A carbonic anhydrase from the nacreous layer in oyster pearls. Proc Natl Acad Sci USA 93:9656–9660

    Article  Google Scholar 

  • Moya A, Tambutté S, Beranger G, Gaume B, Scimeca JC, Allemand D, Zoccola D (2008a) Cloning and use of a coral 36B4 gene to study the differential expression of coral genes between light and dark conditions. Mar Biotechnol NY 10:653–663

    Article  PubMed  CAS  Google Scholar 

  • Moya A, Tambutté S, Bertucci A, Tambutté E, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D (2008b) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization. J Biol Chem 283:25475–25484

    Article  PubMed  CAS  Google Scholar 

  • Puverel S, Tambutté E, Zoccola D, Domart-Coulon I, Bouchot A, Lotto S, Allemand D, Tambutté S (2005) Antibodies against the organic matrix in scleractinians: a new tool to study coral biomineralization. Coral Reefs 24:149–156

    Article  Google Scholar 

  • Rahman MA, Oomori T, Uehara T (2008) Carbonic anhydrase in calcified endoskeleton: novel activity in biocalcification in alcyonarian. Mar Biotechnol (NY) 10:31–38

    Article  CAS  Google Scholar 

  • Supuran CT (2008) Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7:168–181

    Article  PubMed  CAS  Google Scholar 

  • Tambutté 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

    Google Scholar 

  • Tambutté E, Allemand D, Zoccola D, Meibom A, Lotto S, Caminiti N, Tambutté S (2007a) Observations of the tissue-skeleton interface in the scleractinian coral Stylophora pistillata. Coral Reefs 26:517–529

    Article  Google Scholar 

  • Tambutté S, Tambutté E, Zoccola D, Caminiti N, Lotto S, Moya S, Allemand D, Adkins J (2007b) Characterization and role of carbonic anhydrase in the calcification process of the azooxanthellate coral Tubastrea aurea. Mar Biol 151:71–83

    Article  Google Scholar 

  • Venn AA, Tambutté E, Lotto S, Zoccola D, Allemand D, Tambutté S (2009) Imaging intracellular pH in a reef coral and symbiotic anemone. Proc Natl Acad Sci USA 106:16574–16579

    Article  PubMed  CAS  Google Scholar 

  • Weis VM (1993) Effect of dissolved inorganic carbon concentration on the photosynthesis of the symbiotic sea anemone Aiptasia pulchella Carlgren: role of carbonic anhydrase. J Exp Mar Biol Ecol 174:209–225

    Article  CAS  Google Scholar 

  • Weis VM, Reynolds WS (1999) Carbonic anhydrase expression and synthesis in the sea anemone Anthopleura elegantissima are enhanced by the presence of dinoflagellate symbionts. Physiol Biochem Zool 72:307–316

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM (2008) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Nathalie Techer for her technical help and to Dominique Desgré for coral maintenance.

This study was conducted as part of the Centre Scientifique de Monaco Research Programme, supported by the Government of the Principality of Monaco. Anthony Bertucci was supported by a fellowship from the Scientific Centre of Monaco.

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Correspondence to Didier Zoccola.

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Bertucci, A., Tambutté, S., Supuran, C.T. et al. A New Coral Carbonic Anhydrase in Stylophora pistillata . Mar Biotechnol 13, 992–1002 (2011). https://doi.org/10.1007/s10126-011-9363-x

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  • DOI: https://doi.org/10.1007/s10126-011-9363-x

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