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Research Article

Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell

Benjamin Marie, Caroline Joubert, Alexandre Tayalé, Isabelle Zanella-Cléon, Corinne Belliard, David Piquemal, Nathalie Cochennec-Laureau, Frédéric Marin, Yannick Gueguen, and Caroline Montagnani
  1. aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
  2. bUnité Mixte de Recherche 6282 Centre National de la Recherche Scientifique, Biogéosciences, Université de Bourgogne, 21000 Dijon, France;
  3. cCentre Commun de Microanalyse des Protéines, Unité Mixte de Service 344/Unité de Service 8 BioSciences Gerland-Lyon Sud, Institut de Biologie et de Chimie des Protéines, 69007 Lyon, France;
  4. dSkuldtech, 34184 Montpellier, France;
  5. eIfremer, Station de la Trinité-sur-mer, 56470 La Trinité-sur-mer, France; and
  6. fIfremer, Unité Mixte de Recherche 5119 ECOlogie des SYstèmes Marins Côtiers, Université Montpellier II, 34095 Montpellier, France

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PNAS first published December 3, 2012; https://doi.org/10.1073/pnas.1210552109
Benjamin Marie
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
bUnité Mixte de Recherche 6282 Centre National de la Recherche Scientifique, Biogéosciences, Université de Bourgogne, 21000 Dijon, France;
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  • For correspondence: bmarie@mnhn.fr caroline.montagnani@ifremer.fr
Caroline Joubert
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
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Alexandre Tayalé
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
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Isabelle Zanella-Cléon
cCentre Commun de Microanalyse des Protéines, Unité Mixte de Service 344/Unité de Service 8 BioSciences Gerland-Lyon Sud, Institut de Biologie et de Chimie des Protéines, 69007 Lyon, France;
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Corinne Belliard
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
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David Piquemal
dSkuldtech, 34184 Montpellier, France;
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Nathalie Cochennec-Laureau
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
eIfremer, Station de la Trinité-sur-mer, 56470 La Trinité-sur-mer, France; and
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Frédéric Marin
bUnité Mixte de Recherche 6282 Centre National de la Recherche Scientifique, Biogéosciences, Université de Bourgogne, 21000 Dijon, France;
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Yannick Gueguen
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
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Caroline Montagnani
aIfremer, Centre Ifremer du Pacifique, Unité Mixte de Recherche 241 Ecosystèmes Insulaires Océaniens, Tahiti, 98719 Taravao, French Polynesia;
fIfremer, Unité Mixte de Recherche 5119 ECOlogie des SYstèmes Marins Côtiers, Université Montpellier II, 34095 Montpellier, France
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  • For correspondence: bmarie@mnhn.fr caroline.montagnani@ifremer.fr
  1. Edited* by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved October 31, 2012 (received for review July 9, 2012)

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Abstract

Mollusca evolutionary success can be attributed partly to their efficiency to sustain and protect their soft body with an external biomineralized structure, the shell. Current knowledge of the protein set responsible for the formation of the shell microstructural polymorphism and unique properties remains largely patchy. In Pinctada margaritifera and Pinctada maxima, we identified 80 shell matrix proteins, among which 66 are entirely unique. This is the only description of the whole “biomineralization toolkit” of the matrices that, at least in part, is thought to regulate the formation of the prismatic and nacreous shell layers in the pearl oysters. We unambiguously demonstrate that prisms and nacre are assembled from very different protein repertoires. This suggests that these layers do not derive from each other.

  • mantle
  • mollusk shell matrix proteins
  • proteome
  • transcriptome
  • evolution

Footnotes

  • ↵1Present address: Unité Mixte de Recherche 7245 Centre National de la Recherche Scientifique Molécules de Communication et Adaptation des Micro-organismes, Muséum National d'Histoire Naturelle, 75005 Paris, France.

  • ↵2To whom correspondence may be addressed. E-mail: bmarie{at}mnhn.fr or caroline.montagnani{at}ifremer.fr.
  • Author contributions: B.M., N.C.-L., F.M., Y.G., and C.M. designed research; B.M., C.J., A.T., I.Z.-C., C.B., and C.M. performed research; C.J. and A.T. contributed new reagents/analytic tools; B.M., C.J., A.T., I.Z.-C., D.P., F.M., and C.M. analyzed data; and B.M., C.J., F.M., Y.G., and C.M. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. HE610373–HE610410 (P. margaritifera CDS)] and in the Swiss-Prot database [accession nos. P86947–P86969 (P. maxima proteins) and H2A0K6–H2A0P3 (P. margaritifera proteins)].

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1210552109/-/DCSupplemental.

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Nacre versus prisms
Benjamin Marie, Caroline Joubert, Alexandre Tayalé, Isabelle Zanella-Cléon, Corinne Belliard, David Piquemal, Nathalie Cochennec-Laureau, Frédéric Marin, Yannick Gueguen, Caroline Montagnani
Proceedings of the National Academy of Sciences Dec 2012, 201210552; DOI: 10.1073/pnas.1210552109

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Nacre versus prisms
Benjamin Marie, Caroline Joubert, Alexandre Tayalé, Isabelle Zanella-Cléon, Corinne Belliard, David Piquemal, Nathalie Cochennec-Laureau, Frédéric Marin, Yannick Gueguen, Caroline Montagnani
Proceedings of the National Academy of Sciences Dec 2012, 201210552; DOI: 10.1073/pnas.1210552109
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