Advertisement

Mollusk Shells: Does the Nacro-prismatic “Model” Exist?

  • Yannicke Dauphin
  • Jean-Pierre Cuif
Open Access
Conference paper

Abstract

The “nacro-prismatic” shells are the most studied mollusks, and they are often said to be “the” model to unravel the biomineralization mechanisms. Nevertheless, the nacro-prismatic structure is not unique, despite most data are provided by only three genera. The aragonitic nacre is taxon dependent: in cephalopods and gastropods, nacre is columnar, whereas bivalves have a spiral or sheet nacre. The inner structure of gastropod and cephalopod columnar nacre differs. The shape of the tablets is specific of the taxa. Calcitic and aragonitic prisms exist. The composition of the organic matrices extracted from calcitic prisms with a similar shape and mineralogy strongly differs. The inner structure of aragonite prisms is complex, with a central zone and divergent elongated crystallites at the periphery. Additionally, the relationships between nacre and prisms are also taxonomically related. From these data, whatever the scale at which they are studied, every component of the “nacro-prismatic” model – nacre, prisms, and prism–nacre topographic relations – is highly variable, so that this “model” does not exist; it is a structure.

Keywords

Mollusks Nacre Prismatic layer Model 

36.1 Introduction

The most common structure in mollusk shells is the aragonite crossed-lamellar layer, but the most studied is the “nacro-prismatic” arrangement. Almost all data about mollusks are from three bivalve genera with flat large shells: Atrina, Pinna, and Pinctada. These genera are taxonomically related (Pteriomorphia), with large polygonal prismatic units and an inner nacreous layer, so that separating the two layers for detailed analyses is not difficult. They are often used as “the” model to understand the biomineralization processes. Sometimes, Unio and Mytilus, both with a nacro-prismatic structure, are also used as a model. The concept of model to describe this structure suggests that all these nacro-prismatic shells are identical in terms of structure and composition. The examination of the structure and composition of the layers and of the prismatic and nacreous units, as well as their relationships, demonstrates that the nacro-prismatic arrangement is not unique. It is impossible to enter into the detailed description of all mollusk shells. So, the present article will concentrate largely on the differences between the nacro-prismatic shells.

36.2 Materials and Methods

Details about the origin of the samples and preparative process and setup of the diverse used techniques are given in the relevant publications listed in the References.

36.2.1 Materials

Bivalves (Pinctada, Pinna, Nucula, Neotrigonia, Unio), gastropods (Haliotis, Trochus, Turbo), and cephalopods (Nautilus, Sepia, Spirula) were used. Depending on the genera, several species were studied (Pinna, Sepia, Haliotis, among others).

36.2.2 Methods

Micro- and nanostructures were studied using thin sections, fractures, and polished etched surfaces for the scanning electron microscope (secondary and backscattered electron modes, Philips SEM XL30, FEI Phenom) and atomic force microscope (Veeco Nanoscope Dimension 3100). Electron microprobes (energy- and wavelength-dispersive spectrometry) (Link AN10000, CAMECA SX50, SX100) were used for quantitative elemental chemical composition and distribution maps. Chemical distribution maps were also performed using NanoSIMS (CAMECA N50), TOF-SIMS (TOF-SIMS IV Ion-Tof GmbH), and XANES (ID21, ESRF). Thermogravimetric analyses allow to quantify the organic matrix content. Infrared and Raman spectrometry were used on both bulk samples and extracted organic matrices. Liquid chromatography and electrophoresis were used for molecular weights and acidity of the soluble matrices. Lipid content was known using thin-layer chromatography. Amino acid analyses were done on both soluble and insoluble matrices.

36.3 Results

36.3.1 Microstructures

Prisms are aragonite (Neotrigonia, Unionidae, Cephalopoda) or calcite (Pteriomorphia) (Fig. 36.1a–c) (Boggild 1930; Taylor et al. 1969, 1973; Ben Mlih 1983; Checa et al. 2014; Cuif et al. 2011). In some species, calcitic and aragonitic prisms coexist (Dauphin et al. 1989). The inner structure of the prisms is also variable, but the morphological and microstructural diversity is not related to the mineralogy (Sepia, Fig. 36.1b; Haliotis, Fig. 36.1c) but to the taxa. The inner structure of aragonite prisms is complex, with a central zone and divergent elongated crystallites at the periphery. Calcitic prisms are mono- or polycrystalline. The nacre is aragonite, but the tablets are deposited in vertical columns in gastropods and cephalopods, whereas they are in lenses in bivalves (Wise 1970). The inner structure of gastropod and cephalopod columnar nacre differs. Moreover, the shape and the inner structure of the tablets are species dependent (Nautilus, Fig. 36.1d; Pinna, Fig. 36.1e; Sepia, Fig. 36.1f) (Mutvei 1978, 1979). In coleoid cephalopods, the nacreous layer has no tablets (Mutvei 1963) (Fig. 36.1f).
Fig. 36.1

(a) Unetched fracture showing the complex aragonitic prisms of Neotrigonia. (b) Aragonitic prismatic layer of the dorsal shield of Sepia – unetched fracture. (c) Calcitic prisms of Haliotis rufescens, polished and etched fracture. Formic acid 5%, 7 s, 20 °C. (d) Columnar nacreous layer of Nautilus – unetched fracture. (e) Rectangular nacreous tablets of Pinna – unetched sample. (f) Type 2 nacre: layered structure without tablets in a lamella of the ventral part of Sepia – unetched sample. (g) Unetched fracture showing the calcitic prismatic – aragonitic nacreous Fig. 36.1 (continued) transition in Pinctada, with a thick organic membrane and an irregular layer of fibrous aragonite. (h) Aragonitic prism – nacre transition in Neotrigonia – BSE image of a polished and etched section (HCl 1%10 s). (i) BSE map showing the organic membrane and the fibrous aragonite between the calcitic prisms and the nacre in Pinctada. (j) XANES map of S in amino acids in the shell of Pinctada. (k) XANES map of sulfate in Neotrigonia. (l) TOF-SIMS map of alanine in the shell of Pinctada. (m) TOF-SIMS map of glycine of the same section. (n) NanoSIMS map of N in Pinctada. (o): Mg and Sr contents of the prismatic calcitic layers in some species of Haliotis

Not only the shape, mineralogy, and inner structure of the prisms or tablets differ, but the transition between the two layers is also taxonomically dependent. When the prisms are calcite, there is no direct contact between the calcite and the nacre (Cuif et al. 2011). Both layers are separated by a thick organic membrane and an irregular layer of fibrous aragonite (Pinctada, Fig. 36.1g). In shells with aragonitic prisms, the transition is smooth, without an organic membrane (Neotrigonia, Fig. 36.1h) (Dauphin et al. 2014). Chemical differences also exist in the transition zone. Backscattered electron image of the calcitic–aragonitic transition demonstrates that the first aragonitic deposits are not nacre (Pinctada, Fig. 36.1i) (Dauphin et al. 2008). XANES map shows that the chemical composition of the end of the calcitic prisms is modified (Pinctada, Fig. 36.1j) (Dauphin et al. 2003), so that it cannot be said that the termination of prisms is “abrupt” (Hovden et al. 2015). No organic membrane exists between aragonitic prisms and nacre (Neotrigonia, Fig. 36.1k) (Checa and Rodriguez-Navarro 2001; Dauphin et al. 2008, 2014). The amino acid content of the fibrous aragonite differs from that of the nacreous layer, as shown by TOF-SIMS maps (Pinctada, Fig. 36.1l, m) (Farre et al. 2011), and the N map confirms the difference between the nacre and the fibrous aragonite in calcitic–aragonitic shells (Pinctada, Fig. 36.1n) (Dauphin et al. 2008).

It must be added that the elemental chemical composition of a given structure (nacre, calcitic or aragonitic prisms) is species dependent (Fig. 36.1o) (Dauphin et al. 1989).

36.3.2 Organic Components

It is now well-known that mollusk shells are organo-mineral biocomposites. For a given structure, the quantity and nature of the organic matrices differ and depend on the taxa as shown by TGA data of the nacre in Nautilus (Cephalopoda), Trochus (Gastropoda), and Pinctada (Bivalvia) (Fig. 36.2a, b). Insoluble matrices comprise proteins and lipids. It must be noted that the results differ following the sample preparation (decalcification or lipid extraction using organic solvents, Farre and Dauphin 2009). Using the same preparative process, the lipidic composition of the calcitic prisms of Pinna and Pinctada differs (Fig. 36.2c). The molecular weights of the soluble matrices of these prisms also differ (Fig. 36.1d) (Dauphin 2003). As for the insoluble matrices, most analyses are dedicated to the protein contents, mainly amino acid analyses (Pinctada, Nautilus, Fig. 36.2e). Nevertheless, infrared spectrometry of the insoluble matrices shows the presence of lipids and sugars in the insoluble matrices of nacreous layers (Nautilus, Pinctada, Fig. 36.2f). Despite the similarity of shape and mineralogy of the prisms of Pinna and Pinctada, the acidity (pI) and aliphatic index (indicative of the thermal stability for globular proteins) of the insoluble matrices differ (Fig. 36.2g).
Fig. 36.2

(a, b) Thermogravimetric profiles showing the differences in the quantity and composition of the organic matrices in three nacreous layers. (c) Thin-layer chromatography showing the lipidic composition of the calcitic prisms in two bivalve shells. (d) Liquid chromatography of the soluble organic matrices of calcitic prisms. (e) Amino acid composition of the insoluble matrix of nacreous layers. (f) Infrared spectrometry of the insoluble organic matrix of nacreous layers. (g) Isoelectric point (pI) and aliphatic index (alip) of the insoluble organic matrix of calcitic prisms

36.4 Discussion and Conclusion

There is a strong contrast between the small number of studied taxa with a nacro-prismatic structure and the diversity of their shells. The examination of the shape, inner structure, mineralogy, and composition of both mineral and organic components of these shells show the large diversity of these characteristics (Samata 1990), despite some superficial similarities. The relationships between the two layers are also variable and controlled by the organism. However, the diversity is not hazardous: every characteristic is taxonomically dependent, usually at a specific level. Most often, the presence and role of acidic proteins in the biomineralization process is emphasized, but the role of sugars and lipids is neglected (Kocot et al. 2016). Up to now, proteomics and genomics data have not permitted to select the possible mechanisms of the secretion (Suzuki and Nagasawa 2013; Simkiss 2016).

Thus, not only the structure and composition of the nacre and prisms are heterogeneous, they are also dependent on the species, so that this heterogeneity does not suit the usual characteristics of a model. They are neither simple nor unique, so that the nacro-prismatic model concept cannot be sustained.

References

  1. Ben Mlih A (1983) Organisation de la phase carbonatée dans les prismes de Neotrigonia margaritacea Lmk. C R Acad Sci Paris 296(Série III):313–318Google Scholar
  2. Boggild OB (1930) The shell structure of the molluscs. D Kgl Danske Vidensk Selsk Skr, naturvidensk og mathem 9:231–326Google Scholar
  3. Checa AG, Rodriguez-Navarro A (2001) Geometrical and crystallographic constraints determine the self-organization of shell microstructures in Unionidae (Bivalvia: Mollusca). Proc R Soc Lond B 268:771–778CrossRefGoogle Scholar
  4. Checa AG, Salas C, Harper EM, De Dios Bueno-Perez J (2014) Early stage biomineralization in the periostracum of the “living fossil” bivalve Neotrigonia. PLOS ONE 9:2.  https://doi.org/10.1371/journal.pone.0090033 CrossRefGoogle Scholar
  5. Cuif JP, Dauphin Y, Sorauf JE (2011) Biominerals and fossils through time. Cambridge Univ. Press, Cambridge, 490 pGoogle Scholar
  6. 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(17):15168–15177CrossRefGoogle Scholar
  7. Dauphin Y, Cuif JP, Mutvei H, Denis A (1989) Mineralogy, chemistry and ultrastructure of the external shell layer in ten species of Haliotis with reference to Haliotis tuberculata (Mollusca: Archaeogastropoda). Bull Geol Inst Univ Uppsala, NS 15:7–38Google Scholar
  8. Dauphin Y, Cuif JP, Doucet J, Salomé M, Susini J, Williams CT (2003) In situ chemical speciation of sulfur in calcitic biominerals and the simple prism concept. J Struct Biol 142:272–280CrossRefGoogle Scholar
  9. Dauphin Y, Ball AD, Cotte M, Cuif JP, Meibom A, Salomé M, Susini J, Williams CT (2008) Structure and composition of the nacre – prism transition in the shell of Pinctada margaritifera (Mollusca, Bivalvia). Anal Bioanal Chem 390:1659–1169CrossRefGoogle Scholar
  10. Dauphin Y, Cuif JP, Salomé M (2014) Structure and composition of the aragonitic shell of a living fossil: Neotrigonia (Mollusca, Bivalvia). Eur J Mineral 26:485–494CrossRefGoogle Scholar
  11. Farre B, Dauphin Y (2009) Lipids from the nacreous and prismatic layers of two Pteriomorpha mollusc shells. Comp Biochem Physiol B152:103–109CrossRefGoogle Scholar
  12. Farre B, Brunelle A, Laprévote O, Cuif JP, Williams CT, Dauphin Y (2011) Shell layers of the black-lip pearl oyster Pinctada margaritifera: matching microstructure and composition. Comp Biochem Physiol B.  https://doi.org/10.1016/j.cbpb.2011.03.001 CrossRefGoogle Scholar
  13. Hovden R, Wolf SE, Holtz ME, Marin F, Muller DA, Estroff L (2015) Nanoscale assembly processes revealed in the nacroprismatic transition zone of Pinna nobilis mollusc shells. Nature Comm 6:10097.  https://doi.org/10.1038/ncomms10097 CrossRefGoogle Scholar
  14. Kocot KM, McDougall C, Degnan BM (2016) Developing perspectives on molluscan shells, part 1: introduction and molecular biology. In: Saleuddin S, Mukai S (eds) Physiology of molluscs: a collection of selected reviews. CRC PressGoogle Scholar
  15. Mutvei H (1963) On the shells of Nautilus and Spirula with notes on the shell secretion in non-cephalopod molluscs. Arkiv Zool 16:221–227Google Scholar
  16. Mutvei H (1978) Ultrastructural characteristics of the nacre of some gastropods. Zool Scr 7:287–296CrossRefGoogle Scholar
  17. Mutvei H (1979) On the internal structures of the nacreous tablets in molluscan shells. Scan Electron Microsc II:451–462Google Scholar
  18. Samata T (1990) Ca-binding glycoproteins in molluscan shells with different types of ultrastructure. Veliger 33:190–201Google Scholar
  19. Simkiss K (2016) Developing perspectives on molluscan shells, part 2: cellular aspects. In: Saleuddin S, Mukai S (eds) Physiology of molluscs: a collection of selected reviews. CRC PressGoogle Scholar
  20. Suzuki M, Nagasawa H (2013) Mollusk shell structures and their formation mechanism. Can J Zool 91:349–366CrossRefGoogle Scholar
  21. Taylor JD, Kennedy WJ, Hall A (1969) The shell structure and mineralogy of the Bivalvia. I. Introduction. Nuculacae – Trigonacae. Bull Br Mus Nat Hist Zool 3:1–125Google Scholar
  22. Taylor JD, Kennedy WJ, Hall A (1973) The shell structure and mineralogy of the Bivalvia. II. Lucinacea – Clavagellacea. Conclusions. Bull Br Mus nat hist Zool 22:253–294Google Scholar
  23. Wise SWJ (1970) Microarchitecture and mode of formation of nacre (mother-of-pearl) in pelecypods, gastropods and cephalopods. Eclogae Geol Helv 63:775–797Google Scholar

Copyright information

© The Author(s) 2018

Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this book are included in the book's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the book's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

Authors and Affiliations

  1. 1.Institut de systématique, Evolution, Biodiversité, ISYEB – UMR 7205, Muséum national d’Histoire naturelleParisFrance
  2. 2.Centre de recherche sur la paléodiversité et les paléoenvironnements, CR2P – UMR 7207, Muséum national d’Histoire naturelleParisFrance

Personalised recommendations