Journal
ACTA BIOMATERIALIA
Volume 142, Issue -, Pages 194-207Publisher
ELSEVIER SCI LTD
DOI: 10.1016/j.actbio.2022.01.024
Keywords
Biomineralization; Mollusk prisms; Pinctada margaritifera; Pinna nobilis; Coherent raman microscopy; Vectorial ptychography
Funding
- European Research Council (European Union) [724881]
- European Research Council (ERC) [724881] Funding Source: European Research Council (ERC)
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Biomineralization is a complex process bio-controlled by living organisms, involving physical and chemical processes such as ionic concentration regulation and organic molecules production. This study investigates the early-mineralized calcareous units from two bivalve species using advanced optical and X-ray microscopy methods, revealing chemical and crystallographic insights. The observed ring-like structural features in calcite units are correlated with the absence of calcite and an increase in amorphous calcium carbonate and proteins content. Based on these findings, a temporal biomineralization cycle is proposed, providing biomimetic perspectives for designing crystalline materials.
Biomineralization integrates complex physical and chemical processes bio-controlled by the living organ-isms through ionic concentration regulation and organic molecules production. It allows tuning the struc-tural, optical and mechanical properties of hard tissues during ambient-condition crystallisation, motivat-ing 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, Pinc-tada 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 tran-sition 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 forma-tion 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 proper-ties. 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 crys-tallisation 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.(c) 2022 The Author(s). Published by Elsevier Ltd on behalf of Acta Materialia Inc. This is an open access article under the CC BY-NC-ND license ( http://creativecommons.org/licenses/by-nc-nd/4.0/ )
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