Amorphous-to-crystal transition in the layer-by-layer growth of bivalve shell prisms

Type Article
Date 2022-04
Language English
Author(s) Duboisset Julien1, Ferrand Patrick1, Baroni Arthur1, Grünewald Tilman A.ORCID1, Dicko Hamadou1, Grauby OlivierORCID2, Vidal-Dupiol JeremieORCID3, Saulnier Denis4, Le Moullac GillesORCID4, Rosenthal MartinORCID5, Burghammer Manfred5, Nouet JuliusORCID6, Chevallard CorinneORCID7, Baronnet Alain2, Chamard VirginieORCID1
Affiliation(s) 1 : Aix-Marseille Univ, CNRS, Centrale Marseille, Institut Fresnel, Marseille, France
2 : Aix-Marseille Univ, CNRS, CINaM, Campus Luminy, Case 913, 13288-Marseille cedex 9, France
3 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Montpellier France
4 : Ifremer, UMR 241 Environnement Insulaire Océanien (EIO), Labex Corail, Centre du Pacifique, BP 49, Vairao 98719, French Polynesia
5 : European Synchrotron Radiation Facility, F-38043 Grenoble Cedex, France
6 : GEOPS, Univ. Paris-Sud, CNRS, Université Paris-Saclay, 91405 Orsay, France
7 : NIMBE, CEA, CNRS, Université Paris-Saclay, CEA Saclay 91191 Gif-sur-Yvette Cedex, France
Source Acta Biomaterialia (1742-7061) (Elsevier BV), 2022-04 , Vol. 142 , P. 194-207
DOI 10.1016/j.actbio.2022.01.024
WOS© Times Cited 2
Keyword(s) Biomineralization, Mollusk prisms, Pinctada margaritifera, Pinna nobilis, Coherent raman microscopy, Vectorial ptychography

Biomineralization integrates complex physical and chemical processes bio-controlled by the living organisms through ionic concentration regulation and organic molecules production. It allows tuning the structural, optical and mechanical properties of hard tissues during ambient-condition crystallisation, motivating a deeper understanding of the underlying processes. By combining state-of-the-art optical and X-ray microscopy methods, we investigated early-mineralized calcareous units from two bivalve species, Pinctada margaritifera and Pinna nobilis, revealing chemical and crystallographic structural insights. In these calcite units, we observed ring-like structural features correlated with a lack of calcite and an increase of amorphous calcium carbonate and proteins contents. The rings also correspond to a larger crystalline disorder and a larger strain level. Based on these observations, we propose a temporal biomineralization cycle, initiated by the production of an amorphous precursor layer, which further crystallizes with a transition front progressing radially from the unit center, while the organics are expelled towards the prism edge. Simultaneously, along the shell thickness, the growth occurs following a layer-by-layer mode. These findings open biomimetic perspectives for the design of refined crystalline materials.

Statement of Significance

Calcareous biominerals are among the most present forms of biominerals. They exhibit astonishing structural, optical and mechanical properties while being formed at ambient synthesis conditions from ubiquitous ions, motivating the deep understanding of biomineralization. Here, we unveil the first formation steps involved in the biomineralization cycle of prismatic units of two bivalve species by applying a new multi-modal non-destructive characterization approach, sensitive to chemical and crystalline properties. The observations of structural features in mineralized units of different ages allowed the derivation of a temporal sequence for prism biomineralization, involving an amorphous precursor, a radial crystallisation front and a layer-by-layer sequence. Beyond these chemical and physical findings, the herein introduced multi-modal approach is highly relevant to other biominerals and bio-inspired studies.

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Duboisset Julien, Ferrand Patrick, Baroni Arthur, Grünewald Tilman A., Dicko Hamadou, Grauby Olivier, Vidal-Dupiol Jeremie, Saulnier Denis, Le Moullac Gilles, Rosenthal Martin, Burghammer Manfred, Nouet Julius, Chevallard Corinne, Baronnet Alain, Chamard Virginie (2022). Amorphous-to-crystal transition in the layer-by-layer growth of bivalve shell prisms. Acta Biomaterialia, 142, 194-207. Publisher's official version : , Open Access version :