1. Amorphous-to-crystal transition in the layer-by-layer growth of bivalve shell prisms
- Author
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Julien Duboisset, Patrick Ferrand, Arthur Baroni, Tilman A. Grünewald, Hamadou Dicko, Olivier Grauby, Jeremie Vidal-Dupiol, Denis Saulnier, Le Moullac Gilles, Martin Rosenthal, Manfred Burghammer, Julius Nouet, Corinne Chevallard, Alain Baronnet, Virginie Chamard, MOSAIC (MOSAIC), Institut FRESNEL (FRESNEL), Aix Marseille Université (AMU)-École Centrale de Marseille (ECM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-École Centrale de Marseille (ECM)-Centre National de la Recherche Scientifique (CNRS), Coherent Optical Microscopy and X-rays (COMiX), Centre Interdisciplinaire de Nanoscience de Marseille (CINaM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Interactions Hôtes-Pathogènes-Environnements (IHPE), Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Ecosystèmes Insulaires Océaniens (UMR 241) (EIO), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé [Papeete] (ILM), Institut de Recherche pour le Développement (IRD), European Synchroton Radiation Facility [Grenoble] (ESRF), Géosciences Paris Saclay (GEOPS), Institut national des sciences de l'Univers (INSU - CNRS)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Laboratoire Interdisciplinaire sur l'Organisation Nanométrique et Supramoléculaire (LIONS), Nanosciences et Innovation pour les Matériaux, la Biomédecine et l'Energie (ex SIS2M) (NIMBE UMR 3685), Institut Rayonnement Matière de Saclay (IRAMIS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut Rayonnement Matière de Saclay (IRAMIS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS), and European Project: 724881,H2020,3D-BioMat(2017)
- Subjects
Biomineralization ,Technology ,CALCIUM-CARBONATE ,PROTEINS ,Materials Science ,Biomedical Engineering ,02 engineering and technology ,Biochemistry ,Calcium Carbonate ,Pinna nobilis ,Pinctada margaritifera ,Biomaterials ,03 medical and health sciences ,Engineering ,ORGANIC PHASES ,Animals ,Pinctada ,Engineering, Biomedical ,Molecular Biology ,Mollusk prisms ,030304 developmental biology ,Materials Science, Biomaterials ,0303 health sciences ,Science & Technology ,SPECTROSCOPY ,Proteins ,LOCALIZATION ,General Medicine ,021001 nanoscience & nanotechnology ,Bivalvia ,PEARL OYSTER ,STRUCTURE-PROPERTY RELATIONSHIPS ,[PHYS.COND.CM-MS]Physics [physics]/Condensed Matter [cond-mat]/Materials Science [cond-mat.mtrl-sci] ,Vectorial ptychography ,CRYSTALLIZATION ,Coherent raman microscopy ,Crystallization ,0210 nano-technology ,MATRIX ,Biotechnology - Abstract
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 centre, 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 amongst 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. ispartof: ACTA BIOMATERIALIA vol:142 pages:194-207 ispartof: location:England status: published
- Published
- 2022
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