Advertisement

Marine Biotechnology

, Volume 13, Issue 5, pp 992–1002 | Cite as

A New Coral Carbonic Anhydrase in Stylophora pistillata

  • Anthony Bertucci
  • Sylvie Tambutté
  • Claudiu T. Supuran
  • Denis Allemand
  • Didier Zoccola
Original Article

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.

Keywords

Scleractinian corals Carbonic anhydrase Symbiosis Calcification Intracelullar pH 

Notes

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.

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedCrossRefGoogle Scholar
  2. 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 288:1–15CrossRefGoogle Scholar
  3. 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 142:419–426Google Scholar
  4. 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 199:227–248CrossRefGoogle Scholar
  5. 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 25:3389–3402PubMedCrossRefGoogle Scholar
  6. 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 19:650–653PubMedCrossRefGoogle Scholar
  7. 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 17:5054–5058PubMedCrossRefGoogle Scholar
  8. 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 277:87–95PubMedCrossRefGoogle Scholar
  9. 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 18:2300–2303PubMedCrossRefGoogle Scholar
  10. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362PubMedCrossRefGoogle Scholar
  11. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890PubMedCrossRefGoogle Scholar
  12. deBoer ML, Krupp DA, Weis VM (2006) Two atypical carbonic anhydrase homologs from the planula larva of the scleractinian coral Fungia scutaria. Biol Bull 211:18–30PubMedCrossRefGoogle Scholar
  13. Eisenhaber B, Bork P, Eisenhaber F (1999) Prediction of potential GPI-modification sites in proprotein sequences. J Mol Biol 292:741–758PubMedCrossRefGoogle Scholar
  14. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971PubMedCrossRefGoogle Scholar
  15. Erez J (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273:199–202CrossRefGoogle Scholar
  16. 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–R310PubMedGoogle Scholar
  17. 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–R881PubMedGoogle Scholar
  18. Furla P, Galgani I, Durand I, Allemand D (2000b) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457PubMedGoogle Scholar
  19. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131PubMedCrossRefGoogle Scholar
  20. 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 116:59–75CrossRefGoogle Scholar
  21. 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 9:540PubMedCrossRefGoogle Scholar
  22. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  23. 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 5:50–77PubMedCrossRefGoogle Scholar
  24. Huelsenbeck, Ronquist (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  25. Isa Y, Yamazato K (1984) The distribution of carbonic anhydrase in a staghorn coral Acropora hebes (Dana). Galaxea 3:25–36Google Scholar
  26. Jackson DJ, Macis L, Reitner J, Degnan BM, Worheide G (2007) Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis. Science 316:1893–1895PubMedCrossRefGoogle Scholar
  27. 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 246:2561–2573PubMedGoogle Scholar
  28. Kingsley RJ, Watabe N (1987) Role of carbonic anhydrase in calcification in the gorgonian Leptogorgia virgulata. J Exp Zool 241:171–180CrossRefGoogle Scholar
  29. Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255PubMedCrossRefGoogle Scholar
  30. 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 29:309–322CrossRefGoogle Scholar
  31. Lucas JM, Knapp LW (1997) A physiological evaluation of carbon sources for calcification in the octocoral Leptogorgia virgulata (Lamarck). J Exp Biol 200:2653–2662PubMedGoogle Scholar
  32. 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 136:417–426PubMedCrossRefGoogle Scholar
  33. McCall KA, Huang C, Fierke CA (2000) Function and mechanism of zinc metalloenzymes. J Nutr 130:1437S–1446SPubMedGoogle Scholar
  34. 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 93:9656–9660CrossRefGoogle Scholar
  35. 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 10:653–663PubMedCrossRefGoogle Scholar
  36. 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 283:25475–25484PubMedCrossRefGoogle Scholar
  37. 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 24:149–156CrossRefGoogle Scholar
  38. Rahman MA, Oomori T, Uehara T (2008) Carbonic anhydrase in calcified endoskeleton: novel activity in biocalcification in alcyonarian. Mar Biotechnol (NY) 10:31–38CrossRefGoogle Scholar
  39. Supuran CT (2008) Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7:168–181PubMedCrossRefGoogle Scholar
  40. Tambutté E, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041Google Scholar
  41. 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 26:517–529CrossRefGoogle Scholar
  42. 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 151:71–83CrossRefGoogle Scholar
  43. 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 106:16574–16579PubMedCrossRefGoogle Scholar
  44. 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 174:209–225CrossRefGoogle Scholar
  45. 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 72:307–316PubMedCrossRefGoogle Scholar
  46. Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM (2008) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Anthony Bertucci
    • 1
  • Sylvie Tambutté
    • 1
  • Claudiu T. Supuran
    • 2
  • Denis Allemand
    • 1
  • Didier Zoccola
    • 1
  1. 1.Centre Scientifique de MonacoMonacoMonaco
  2. 2.Dipartimento di ChimicaUniversity of FlorenceSesto Fiorentino (Florence)Italy

Personalised recommendations