Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-23T23:14:09.427Z Has data issue: false hasContentIssue false

Is the pearl layer a reversed shell? A re-examination of the theory of pearl formation through physical characterizations of pearl and shell developmental stages in Pinctada margaritifera

Published online by Cambridge University Press:  24 November 2011

Jean-Pierre Cuif*
Affiliation:
UMR 8148 IDES, bât. 504, Sciences de la Terre, Université Paris Sud, 91405 Orsay, France
Yannicke Dauphin
Affiliation:
UMR 8148 IDES, bât. 504, Sciences de la Terre, Université Paris Sud, 91405 Orsay, France
Lauren Howard
Affiliation:
Natural History Museum, Cromwell Road, London, SW7 5BD, UK
Julius Nouet
Affiliation:
UMR 8148 IDES, bât. 504, Sciences de la Terre, Université Paris Sud, 91405 Orsay, France
Stéphan Rouzière
Affiliation:
UMR 8502, Physique des Solides, Bât. 510, Université Paris Sud, 91405 Orsay, France
Murielle Salomé
Affiliation:
ID21, European Synchrotron Radiation Facility, BP 220, 38043 Grenoble, France
*
aCorresponding author: jean-pierre.cuif@u-psud.fr
Get access

Abstract

A series of physical characterization methods (UV fluorescence microscopy, X-ray microdiffraction, backscattered electron imaging and X-ray absorption spectroscopy) were applied to Polynesian pearls collected after different cultivation periods, varying from three weeks to eighteen months. Through this rigorous time-based sampling, 120 pearls produced by 20 different donor oysters were compared. Results show that the structure of the pearl layer can be understood as a sequence of distinct secretion processes whose progressive occurrence through time may lead to variously arranged and sometimes aberrant mineralized structures. By making comparisons with the structure and growth mode of the Pinctada margaritifera shell, this study shows that the currently accepted theory that views the pearl-bed as a “reversed shell” cannot account for the diversity of the microstructural patterns and mineralogical properties observed in the pearl layers. From a practical and economic view point, it appears that development of these pre-nacreous materials superposed onto a perfectly round-shaped nucleus is the main cause of shape irregularities in pearls and the consequent decrease in their value.

Type
Research Article
Copyright
© EDP Sciences, IFREMER, IRD 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnaud-Haond, S., Goyard, E., Vonau, V., Herbaut, C., Prou, J., Saulnier, D., 2007, Pearl formation: persistence of the graft during the entire process of biomineralization. Mar. Biotechnol. 9, 113116. CrossRefGoogle ScholarPubMed
Baronnet, A., Cuif, J.P., Dauphin, Y., Farre, B., Nouet, J., 2008, Crystallization of biogenic Ca-carbonate within organo-mineral micro-domains. Structure of the calcite prisms of the pelecypod Pinctada margaritifera (Mollusca) at the submicron to nanometer ranges. Mineral. Mag. 72, 617626. CrossRefGoogle Scholar
Cuif, J.P., Ball, A.D., Dauphin, Y., Farre, B., Nouet, J., Perez-Huerta, A., Salomé, M., Williams, C.T., 2008, Structural, mineralogical and biochemical diversity in the lower part of the pearl layer of cultivated seawater pearls from Polynesia. Microsc. Microanal. 14, 405417. CrossRefGoogle ScholarPubMed
Cuif J.P., Dauphin Y., Sorauf J.E., 2011, Biominerals and fossils through time. Cambridge University Press.
Cuif, J.P., Dauphin, Y., Doucet, J., Salomé, M., Susini, J., 2003, XANES mapping of organic sulfate in three scleractinian coral skeletons. Geoch. Cosmoch. Acta, 67, 7583. CrossRefGoogle Scholar
Dauphin, Y., 2003, Soluble organic matrices of the calcitic prismatic shell layers of two pteriomorphid Bivalves: Pinna nobilis and Pinctada margaritifera. J. Biol. Chem. 278, 1516815177. CrossRefGoogle ScholarPubMed
Dauphin, Y., Cuif, J.P., Doucet, J., Salomé, M., Susini, J., Williams, C.T., 2003a, In situ chemical speciation of sulfur in calcitic biominerals and the simple prism concept. J. Struct. Biol. 142, 272280. CrossRefGoogle ScholarPubMed
Dauphin, Y., Cuif, J.P., Doucet, J., Salomé, M., Susini, J., Williams, C.T., 2003b, In situ mapping of growth lines in the calcitic prismatic layers of mollusc shells using X-ray absorption near-edge structure (XANES) spectroscopy at the sulphur edge. Mar. Biol. 142, 299304. CrossRefGoogle Scholar
Dauphin, Y., Ball, A.D., Cotte, M., Cuif, J.P., Meibom, A., Salomé, M., Susini, J., Williams, C.T., 2008, Structure and composition of the nacre – prism transition in the shell of Pinctada margaritifera (Mollusca, Bivalvia). Anal. Bioanal. Chem. 390, 16591169. CrossRefGoogle Scholar
Dauphin, Y., Brunelle, A., Cotte, M., Cuif, J.P., Farre, B., Laprévote, O., Meibom, A., Salomé, M., Williams, C.T., 2010, A layered structure in the organic envelopes of the prismatic layer of the shell of the pearl oyster Pinctada margaritifera (Mollusca, Bivalvia). Microsc. Microanal. 16, 9198 CrossRefGoogle Scholar
Farre, B., Brunelle, A., Laprévote, O., Cuif, J.P., Williams, C.T., Dauphin, Y., 2011, Shell layers of the black-lip pearl oyster Pinctada margaritifera: matching microstructure and composition. Comp. Biochem. Physiol. B 159, 131139. CrossRefGoogle ScholarPubMed
Fryda, J., Kliknarova, K., Frydiva, B., Mergl, M., 2010, Variability in the crystallographic texture of bivalve nacre. Bull. Geosci. 85, 645662. CrossRefGoogle Scholar
Inoue, N., Ishibashi, R., Ishikawa, T., Atsumi, T., Aoki, H., Komaru, A., 2011, Can the quality of pearls from the Japanese pearl oyster (Pinctada fucata) be explained by the gene expression patterns of the major shell matrix proteins in the pearl sac? Mar. Biotechnol. 13, 4855. Google Scholar
Joubert C., Piquemal D., Maris B., Manchon L., Pierrat F., Zanella-Clleaon I., Cochennec-Laureau N., Guegen Y., Montgnani C., 2010, Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11, 613 doi: 10.11861471-2164-11-613.
Kawakami, I.K., 1952a, Studies on pearl formation. On the regeneration and transformation of the mantle piece in the pearl oyster. Mem. Fac. Kyushu Univ., Ser. E 1, 8389. Google Scholar
Kawakami, I.K., 1952b, Marine regeneration in pearl oyster (Pinctada martensii). J. Fuji Pearl. Inst. 2(2), 14. Google Scholar
Kobayashi, I., 2008, Scanning electron microscopic structure of the prismatic layer in the Bivalvia. Front. Mater. Sci. China 2, 246252. CrossRefGoogle Scholar
Kong, Y., Jing, G., Yan, Z., Li, C., Gong, N., Zhu, F., Li, D., Zhang, Y., Zheng, G., Wang, H., Xie, L., Zhang, R., 2009, Cloning and characterization of prisilkin-39, a novel matrix protein serving a dual role in the prismatic layer formation from the oyster Pinctada fucata. J. Biol. Chem. 284, 1084210854. CrossRefGoogle Scholar
Nudelman, F., Shimoni, E., Klein, E. ,Rousseau, M., Bourrat, X., Lopez, E., Addadi, L., Weiner, S., 2008, Forming nacreous layer of the shells of the bivalves Atrina rigida and Pinctada margaritifera: an environmental- and cryoscanning electron microscopy study. J. Struct. Biol. 162, 290300. CrossRefGoogle Scholar
Okumura, T., Suzuki, M., Nagasawa, H., Kogure, T., 2010, Characteristics of biogenic calcite in the prismatic layer of a pearl oyster, Pinctada fucata. Micron 41, 821826. CrossRefGoogle ScholarPubMed
Rouzière, S., Jourdanneau, E., Kasmi, B., Petermann, D., Albouy, P.A., 2010, A laboratory X-ray microbeam for combined X-ray diffraction and fluorescence measurements. J. Appl. Cryst. 43, 11311133. CrossRefGoogle Scholar
Saleuddin, A.S.M., 1974, An electron microscopic study of the formation and structure of the periostracum in Astarte (Bivalvia). Rev. Can. Zool. 52, 14631471. CrossRefGoogle Scholar
Schâffer, T.E., Ionescu-Zanetti, C., Proksch, R., Fritz, M., Walters, D.A., Almquist, N., Zaremba, C., Belcher, A.M, Smith, B.L., Stucky, G.D., Morse, D.E., Hansma, P.K., 1997, Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges. Chem. Mater. 9, 17311740. CrossRefGoogle Scholar
Suzuki, S., Uozumi, S., 1981, Organic components of prismatic layers in molluscan shells. J. Fac. Sci. Hokkaido Univ., Ser. IV. 20, 720. Google Scholar
Suzuki, M., Sakuda, S., Nagasawa, H., 2007, Identification of chitin in the prismatic layer of the shell and a chitin synthase gene from the Japanese pearl oyster, Pinctada fucata. Biosci. Biotechnol. Biochem. 71, 17351744. CrossRefGoogle Scholar
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, 5946, 13881390. CrossRefGoogle ScholarPubMed
Tagaki, R., Miyashita, T., 2010, Prismin: A new matrix protein family in the Japanese pearl oyster (Pinctada fucata) involved in prismatic layer formation. Zool. Sci. 27, 416426. CrossRefGoogle Scholar
Taylor, J.D., Kennedy, W.J., Hall, A., 1969, The shell structure and mineralogy of the Bivalvia. I. Introduction. Nuculacae–Trigonacae. Bull. Br. Mus. Nat. Hist. Zool. 3, 1125. Google Scholar
Taylor J., Strack E., 2008, Pearl production. In: Southgate P.C., Lucas J.S. (Eds.). The pearl oyster, Amsterdam, Elsevier, pp. 272–302.
Tsukamoto, D., Sarashina, I., Endo, K., 2004, Structure and expression of an unusually acidic matrix protein of pearl oyster shells. Biochem. Biophys. Res. Comm. 320, 11751180. CrossRefGoogle Scholar
Zhang, C., Xie, L., Huang, J., Liu, X., Zhang, R., 2006, A novel matrix protein family participating in the prismatic layer framework formation of pearl oyster, Pinctada fucata. Biochem. Biophys. Res. Comm. 344, 735740. CrossRefGoogle ScholarPubMed
Aquat. Living Resour. 23, 277–284 (2010)