The skeletal proteome of the coral acropora millepora: The evolution of calcification by co-option and domain shuffling

Molecular Biology and Evolution

Volumn 30, Issue 9, 2013, Pages 2099-2112

  Ramos Silva, Paula ^a,b   Kaandorp, Jaap ^b   Huisman, Lotte ^b,c   Marie, Benjamin ^d   Zanella Cléon, Isabelle ^e   Guichard, Nathalie ^a   Miller, David J ^c   Marin, Frédéric ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c JAMES COOK UNIVERSITY   (Australia)

^d MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^e University Lyon i   (France)

Author keywords

biomineralization; calcium carbonate skeleton; evolution; proteomics; scleractinian

Indexed keywords

ACID PROTEIN; ACIDIC SOMP PROTEIN; CALCIUM CARBONATE; CEPHALOTOXIN LIKE PROTEIN; COADHESIN; COLLAGEN TYPE 1 ALPHA 1; CUB DOMAIN CONTAINING PROTEIN; ECTIN; EGF AND LAMININ G DOMAIN CONTAINING PROTEIN; EPIDERMAL GROWTH FACTOR; GLUTAMIC ACID RICH PROTEIN; HEPHAESTIN; HEPHAESTIN LIKE PROTEIN; MAM AND FIBRONECTIN CONTAINING PROTEIN; MATRIX PROTEIN; MEMBRANE PROTEIN; MEPRIN; MUCIN; NEUROGLIAN LIKE PROTEIN; POLYCYSTIC KIDNEY DISEASE 1 RELATED PROTEIN; PROTEOME; PROTOCAHERIN LIKE PROTEIN; PUTATIVE CARBONIC ANHYDRASE; SECRETED ACIDIC PROTEIN 1; SECRETED ACIDIC PROTEIN 2; SKELETAL ASPARTIC ACID RICH PROTEIN 1; SKELETAL ASPARTIC ACID RICH PROTEIN 2; SOM MAM AND LDL RECEPTOR 1 PROTEIN; SOM MAM AND LDL RECEPTOR 2 PROTEIN; THREONINE RICH PROTEIN; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; BIOINFORMATICS; CORAL; DOMAIN SHUFFLING; EPITHELIUM; EVOLUTION; EXTRACELLULAR MATRIX; MASS SPECTROMETRY; PROTEIN ANALYSIS; PROTEOMICS; SKELETON; TRANSCRIPTOMICS;

EID: 84883230158     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst109     Document Type: Article

References (105)

1. Addadi L, Moradian J, Shay E, Maroudas NG,Weiner S. 1987. A chemical model for the cooperation of sulfates and carboxylates in calcite crystal nucleation: relevance to biomineralization. Proc Natl Acad Sci USA. 84:2732-2736.
2. Allemand D, Tambutté É, Zoccola D, Tambutté S. 2011. Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N, editors. Coral reefs: an ecosystem in transition. Dordrecht (The Netherlands): Springer. p. 119-150.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
4. Ball EE, Hayward DC, Saint R, Miller DJ. 2004. A simple plan-cnidarians and the origins of developmental mechanisms. Nat Rev Genet. 5: 567-577.
5. Bayer T, Aranda M, Sunagawa S, Yum LK, Desalvo MK, Lindquist E, Coffroth MA, Voolstra CR, Medina M. 2012. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PloS One 7:e35269.
6. Bertucci A, Tambutté S, Supuran CT, Allemand D, Zoccola D. 2011. A new coral carbonic anhydrase in Stylophora pistillata. Mar Biotechnol. 13:992-1002.
7. Bieber AJ, Snow PM, Hortsch M, Patel NH, Jacobs JR, Traquina ZR, Schilling J, Goodman CS. 1989. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59:447-460.
8. Bork P. 1992. Mobile modules and motifs. Curr Opin Struct Biol. 2: 413-421.
9. Brinkman DL, Mulvenna J, Konstantakopoulos N, Hodgson WC, Isbister GK, Seymour JE, Burnell JN. 2012. 106 Molecular diversity of box jellyfish toxins. Toxicon 60:148-149.
10. Brown BE, Tudhope AW, Le Tissier MDA, Scoffin TP. 1991. A novel mechanism for iron incorporation into coral skeletons. Coral Reefs 10:211-215.
11. Caldeira K, Wickett ME. 2003. Anthropogenic carbon and ocean pH. Nature 425:365.
12. Chan NCS, Connolly SR. 2013. Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol. 19:282-290.
13. Cohen AL, McConnaughey TA. 2003. Geochemical perspectives on coral mineralization. Rev Mineral Geochem. 54:151-188.
14. Cohen AL, McCorkle DC, De Putron S, Gaetani GA, Rose KA. 2009. Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochem Geophys Geosyst. 10: Q07005, doi:10.1029/ 2009GC002411.
15. Collins AG. 2002. Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J Evolution Biol. 15:418-432.
16. Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M. 2006. Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol. 55:97-115.
17. Constantz B,Weiner S. 1988. Acidic macromolecules associated with the mineral phase of scleractinian coral skeletons. J Exp Zool. 248: 253-258.
18. Cuif J-P, Dauphin Y, Gautret P. 1999. Compositional diversity of soluble mineralizing matrices in some recent coral skeletons compared to fine-scale growth structures of fibres: discussion of consequences for biomineralization and diagenesis. Int J Earth Sci. 88:582-592.
19. Cuif J-P, Dauphin Y, Freiwald A, Gautret P, Zibrowius H. 1999. Biochemical markers of zooxanthellae symbiosis in soluble matrices of skeleton of 24 Scleractinia species. Comp Biochem Physiol Part A Mol Integr Physiol. 123:269-278.
20. Cusack M, Freer A. 2008. Biomineralization: elemental and organic influence in carbonate systems. Chem Rev. 108:4433-4454.
21. Dauphin Y, Cuif JP. 1997. Isoelectric properties of the soluble matrices in relation to the chemical composition of some Scleractinian skeletons. Electrophoresis 18:1180-1183.
22. De'ath G, Lough JM, Fabricius KE, 2009, Declining coral calcification on the Great Barrier Reef. Science, 323, 116-119.
23. Debreuil J, Tambutté E, Zoccola D, Deleury E, Guigonis J-M, Samson M, Allemand D, Tambutté S. 2012. Molecular cloning and characterization of first organic matrix protein from sclerites of red coral, Corallium rubrum. J Biol Chem. 287:19367-19376.
24. Doolittle RF. 1992. Reconstructing history with amino acid sequences. Proteome Sci. 1:191-200.
25. Drake JL, Mass T, Haramaty L, Zelzion E, Bhattacharya D, Falkowski PG. 2013. Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. Proc Natl Acad Sci USA. 110:3788-3793.
26. Engel J. 1991. Common structural motifs in proteins of the extracellular matrix. Curr Opin Cell Biol. 3:779-785.
27. Falini G, Reggi M, Fermani S, Sparla F, Goffredo S, Dubinsky Z, Levi O, Dauphin Y, Cuif J-P. 2013. Control of aragonite deposition in colonial corals by intra-skeletal macromolecules. J Struct Biol. pii:S1047-8477 (13)00115-9.
28. Farre B, Cuif J-P, Dauphin Y. 2010. Occurrence and diversity of lipids in modern coral skeletons. Zoology 113:250-257.
29. Frank M, Kemler R. 2002. Protocadherins. Curr Opin Cell Biol. 14: 557-562.
30. Frazão B, Vasconcelos V, Antunes A. 2012. Sea anemone (Cnidaria, Anthozoa, Actiniaria) toxins: an overview. Mar Drugs. 10:1812-1851.
31. Fukuda I, Ooki S, Fujita T, Murayama E, Nagasawa H, Isa Y, Watanabe T. 2003. Molecular cloning of a cDNA encoding a soluble protein in the coral exoskeleton. Biochem Biophys Res Commun. 304:11-17.
32. Gaffey SJ, Bronnimann CE. 1993. Effects of bleaching on organic and mineral phases in biogenic carbonates. J Sediment Res. 63: 752-754.
33. Gattuso J-P, Frankignoulle M, Wollast R. 1998. Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu Rev Ecol Syst. 29: 405-434.
34. Geffen Y, Ron EZ, Rosenberg E. 2009. Regulation of release of antibacterials from stressed scleractinian corals. FEMS Microbiol Lett. 295: 103-109.
35. Glimcher M. 1959. Molecular biology of mineralized tissues with particular reference to bone. Rev Mod Phys. 31:359-393.
36. Gochfeld D, Aeby G. 2008. Antibacterial chemical defenses in Hawaiian corals provide possible protection from disease. Mar Eco Prog Ser. 362:119-128.
37. Goffredo S, Vergni P, Reggi M, Caroselli E, Sparla F, Levy O, Dubinsky Z, Falini G. 2011. The skeletal organic matrix from Mediterranean coral Balanophyllia europaea influences calcium carbonate precipitation. PLoS One 6:e22338.
38. Goldberg WM. 1974. Evidence of a sclerotized collagen from the skeleton of a gorgonian coral. Comp Biochem Physiol B Comp Biochem. 49:525-529.
39. Goldberg WM. 2001. Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi. Tissue Cell 33:376-387.
40. Helman Y, Natale F, Sherrell RM, Starovoytov V, Gorbunov MY, Falkowski PG. 2008. Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro. Proc Natl Acad Sci USA. 105:54-58.
41. Hincke MT, Gautron J, Panheleux M, Garcia-ruiz J, Mckee MD. 2000. Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biol. 19: 443-453.
42. Ingalls AE, Lee C, Druffel ER. 2003. Preservation of organic matter in mound-forming coral skeletons. Geochim Cosmochim Acta. 67: 2827-2841.
43. Isa Y, Yamazato K. 1984. The distribution of carbonic anhydrase in a staghorn coral, Acropora hebes (Dana). Galaxea 3:25-36.
44. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M. 2005. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics. 4: 1265-1272.
45. Jonchère V, Réhault-Godbert S, Hennequet-Antier C, Cabau C, Sibut V, Cogburn LA, Nys Y, Gautron J. 2010. Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics 11:57.
46. Joseph JM, Durand D. 2009. Family classification without domain chaining. Bioinformatics 25:i45-i53.
47. Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cléon I, Cochennec-Laureau N, Gueguen Y, Montagnani C. 2010. Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11:613.
48. Kingsley RJ, Tsuzaki M, Watabe N, Mechanic GL. 1990. Collagen in the spicule organic matrix of the gorgonian Leptogorgia virgulata. Biol Bull. 179:207-213.
49. Kleypas JA, Yates KK. 2009. Coral reefs and ocean acidification. Oceanography 22:108-117.
50. Kline DI, Teneva L, Schneider K, et al. (24 co-authors). 2012. A shortterm in situ CO2 enrichment experiment on Heron Island (GBR). Sci Rep. 2:1-9.
51. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J-P. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol. 19:1884-1896.
52. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
53. LangM, Braun CL, KanostMR, Gorman MJ. 2012. Multicopper oxidase-1 is a ferroxidase essential for iron homeostasis in Drosophila melanogaster. Proc Natl Acad Sci USA. 109:13337-13342.
54. Langdon C, Atkinson MJ. 2005. Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res. 110:1-16.
55. Mann K, Macek B, Olsen JV. 2006. Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 6: 3801-3810.
56. Mann K, Poustka AJ, Mann M. 2008a. In-depth, high-accuracy proteomics of sea urchin tooth organic matrix. Prot Sci. 6:33.
57. Mann K, Poustka AJ, Mann M. 2008b. The sea urchin (Strongylocentrotus purpuratus) test and spine proteomes. Prot Sci. 10:1-10.
58. Mann K, Wilt FH, Poustka AJ. 2010. Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix. Prot Sci. 8:1-12.
59. Marie B, Jackson DJ, Ramos-Silva P, Zanella-Cléon I, Guichard N, Marin F. 2013. The shell-forming proteome of Lottia gigantea reveals both deep conservations and lineage specific novelties. FEBS J. 280: 214-232.
60. Marie B, Joubert C, Tayalé A, Zanella-Cléon I, Belliard C, Piquemal D, Cochennec-Laureau N, Marin F, Gueguen Y, Montagnani C. 2012. Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell. Proc Natl Acad Sci USA. 109:20986-20991.
61. Marie B, Marin F, Marie A, Bédouet L, Dubost L, Alcaraz G, Milet C, Luquet G. 2009. Evolution of nacre: biochemistry and proteomics of the shell organic matrix of the cephalopod Nautilus macromphalus. ChemBioChem. 10:1495-1506.
62. Marie B, Zanella-Cléon I, Le Roy N, Becchi M, Luquet G, Marin F. 2010. Proteomic analysis of the acid-soluble nacre matrix of the bivalve Unio pictorum: detection of novel carbonic anhydrase and putative protease inhibitor proteins. ChemBioChem. 11: 2138-2147.
63. Marin F, Corstjens P, De Gaulejac B, De Vrind-De Jong E, Westbroek P. 2000. Mucins and molluscan calcification. Molecular characterization of mucoperlin, a novel mucin-like protein from the nacreous shell layer of the fan mussel Pinna nobilis (Bivalvia, pteriomorphia). J Biol Chem. 275:20667-20675.
64. Marin F, Le Roy N, Marie B. 2012. The formation and mineralization of mollusk shell. Front Biosci (Schol Ed). 4:1099-1125.
65. Marin F, Luquet G. 2007. Unusually acidic proteins in biomineralization. In: Bauerlein E, editor. Handbook of biomineralization-biological aspects and structure formation.Weinheim (Germany):Wiley-VCH. p. 273-90.
66. Marin F, Pereira L, Westbroek P. 2001. Large-scale fractionation of molluscan shell matrix. Protein Expr Purif. 23:175-179.
67. Maurer P, Hohenester E, Engel J. 1996. Extracellular calcium-binding proteins. Curr Opin Cell Biol. 8:609-617.
68. Meyer E, Aglyamova GV, Matz MV. 2011. Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol Ecol. 20:3599-3616.
69. Miksík I, Sedláková P, Lacinová K, Pataridis S, Eckhardt A. 2010. Determination of insoluble avian eggshell matrix proteins. Anal Bioanal Chem. 397:205-214.
70. Milliman JD, Droxler AW. 1996. Neritic and pelagic carbonate sedimentation in the marine environment: ignorance is not bliss. Geologische Rundschau. 85:496-504.
71. Mitterer RM. 1978. Amino acid composition and metal binding capability of the skeletal protein of corals. Bull Mar Sci. 28:173-180.
72. 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. 93:9657-9660.
73. Morrissey JH. 1981. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 117:307-310.
74. Mosher DF, Adams JC. 2012. Adhesion-modulating/matricellular ECM protein families: a structural, functional and evolutionary appraisal. Matrix Biol. 31:1-7.
75. Moya A, Huisman L, Ball EE, Hayward DC, Grasso LC, Chua CM, Woo HN, Gattuso J.-P, Forêt S, Miller DJ. 2012. Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO(2)-driven acidification during the initiation of calcification. Mol Ecol. 21:2440-2454.
76. Moya A, Tambutté S, Bertucci A, Tambutté E, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D. 2008. Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization. J Biol Chem. 283:25475-25484.
77. Orr JC, Fabry VJ, Aumont O, et al. (28 co-authors). 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681-686.
78. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:418-422.
79. Ptitsyn A, Moroz LL. 2012. Computational workflow for analysis of gain and loss of genes in distantly related genomes. BMC Bioinformatics 13(1 Suppl):S5.
80. Puverel S, Tambutté E, Pereira-Mouriès L, Zoccola D, Allemand D, Tambutté S. 2005. Soluble organic matrix of two Scleractinian corals: partial and comparative analysis. Comp Biochem Physiol B Biochem Mol Biol. 141:480-487.
81. Rahman MA, Isa Y. 2005. Characterization of proteins from thematrix of spicules from the alcyonarian, Lobophytum crassum. J ExpMar Biol Ecol. 321:71-82.
82. Rahman MA, Isa Y, Takemura A, Uehara T. 2006. Analysis of proteinaceous components of the organic matrix of endoskeletal sclerites from the alcyonarian Lobophytum crassum. Calcif Tissue Int. 78: 178-185.
83. Rahman MA, Isa Y, Uehara T. 2005. Proteins of calcified endoskeleton: II partial amino acid sequences of endoskeletal proteins and the characterization of proteinaceous organic matrix of spicules from the alcyonarian, Synularia polydactyla. Proteomics 5:885-893.
84. Rahman MA, Isa Y, Uehara T. 2006. Studies on two closely related species of octocorallians: biochemical and molecular characteristics of the organic matrices of endoskeletal sclerites. Mar Biotechnol (NY). 8:415-424.
85. Ramos-Silva P, Benhamada S, Le Roy N, et al. (11 co-authors). 2012. Novel molluskan biomineralization proteins retrieved from proteomics: a case study with Upsalin. ChemBioChem. 13:1067-1078.
86. Ramos-Silva P, Marin F, Kaandorp J, Marie B. 2013. Biomineralization toolkit: The importance of sample cleaning prior to the characterization of biomineral proteomes. Proc Natl Acad Sci USA. 110: E2144-E2146.
87. Reyes-Bermudez A, Lin Z, Hayward DC, Miller DJ, Ball EE. 2009. Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora. BMC Evol Biol. 9:178.
88. Shinzato C, Shoguchi E, Kawashima T, et al. (13 co-authors). 2011. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320-323.
89. Song N, Joseph JM, Davis GB, Durand D. 2008. Sequence similarity network reveals common ancestry of multidomain proteins. PLoS Comput Biol. 4:e1000063.
90. Stolarski J, KitaharaMV, Miller DJ, Cairns SD, MazurM,Meibom A. 2011. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol Biol. 11:316.
91. Sunagawa S, DeSalvo MK, Voolstra CR, Reyes-Bermudez A, Medina M. 2009. Identification and gene expression analysis of a taxonomically restricted cysteine-rich protein family in reef-building corals. PLoS One 4:e4865.
92. Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, Nagasawa H. 2009. An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 325:1388-1390.
93. Tambutté S, Tambutté E, Zoccola D, Allemand D. 2008. Organic matrix and biomineralization of scleractinian corals. In: Bauerlein E, editor. Handbook of biomineralization-biological aspects and structure formation. Weinheim (Germany): Wiley-VCH. p. 243-259.
94. Tambutté S, Tambutté E, Zoccola D, Caminiti N, Lotto S, Moya A, Allemand D, Adkins J. 2006. Characterization and role of carbonic anhydrase in the calcification process of the azooxanthellate coral Tubastrea aurea. Mar Biol. 151:71-83.
95. Ueda A, Nagai H, Ishida M, Nagashima Y, Shiomi K. 2008. Purification and molecular cloning of SE-cephalotoxin, a novel proteinaceous toxin from the posterior salivary gland of cuttlefish Sepia esculenta. Toxicon 52:574-581.
96. Van Oppen MJ, McDonald BJ,Willis B, Miller DJ. 2001. The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol. 18: 1315-1329.
97. Veis A. 2011. Organic matrix-related mineralization of sea urchin spicules, spines, test and teeth. Front Biosci. 16:2540.
98. Veis A, Sabsay B. 1987. The collagen of mineralized matrices. In: Peck WA, editor. Bone and mineral research, Vol. 5. New York (NY): Elsevier Science. p. 15.
99. Vulpe CD, Kuo YM, Murphy TL, Cowley L, Askwith C, Libina N, Gitschier J, Anderson GJ. 1999. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the slamouse. Nat Genet. 21:195-199.
100. Wheeler AP, George JW, Evans CA. 1981. Control of calcium carbonate nucleation and crystal growth by soluble matrx of oyster shell. Science 212:1397-1398.
101. Wilbur K, Saleuddin AS. 1983. Shell formation. In: Wilbur K, Saleuddin AS, editors. The Mollusca. Vol. 4. Physiology, Part 1. New York: Academic Press. p. 235-287.
102. Wootton JC, Federhen S. 1993. Statistics of local complexity in amino acid sequences and sequence databases. Computers Chem. 17: 149-163.
103. Zhang G, Fang X, Guo X, et al. (85 co-authors). 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49-54.
104. Zoccola D, Moya A, Béranger GE, Tambutté E, Allemand D, Carle GF, Tambutté S. 2009. Specific expression of BMP2/4 ortholog in biomineralizing tissues of corals and action on mouse BMP receptor. Mar Biotechnol. 11:260-269.
105. Zoccola D, Tambutté E, Kulhanek E, Puverel S, Scimeca J-C, Allemand D, Tambutté S. 2004. Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. Biochim Biophys Acta. 1663:117-126.