Interplay between Calcite, Amorphous Calcium Carbonate, and Intracrystalline Organics in Sea Urchin Skeletal Elements

Abstract

Biomineralization processes in living organisms result in the formation of skeletal elements with complex ultrastructures. Although the formation pathways in sea urchin larvae are known, the interrelation between calcite, amorphous calcium carbonate (ACC), and intra-crystalline organics in adult sea urchin biominerals is less clear. Here, we study this interplay in the spines and test 2 plates of the Paracentrotus lividus sea urchins whose skeletal elements have optimized functionproperties relationships. Thermogravimetric analysis coupled with differential scanning calorimetry or mass spectrometry measurements, nuclear magnetic resonance technique and high-resolution powder X-ray diffraction show that pristine spines and test plates are composed of Mg-rich calcite and comprise about 10 wt. % of anhydrous ACC, 1.2 to 1.6 wt. % of organics, and less than 0.2 wt. % of water. Anhydrous ACC originates from incomplete crystallization of a precursor ACC phase during biomineralization and is associated with intra-crystalline organics at the molecular level. Molecular interactions at organic/inorganic interfaces cause significant calcite lattice distortions of the tensile type. The latter are amplified during ACC crystallization and finally disappear after heat-assisted destruction of organic molecules. Converting the measured lattice distortions (strains) into internal stress components, we follow stress evolution upon annealing and find that complete crystallization of ACC leads to the isotropy of residual stresses in all investigated skeletal parts. These results allow us to speculate that organic macromolecules are preferentially attached to different crystallographic planes in the pristine test and spine samples.

Origin of the biphase nature and surface roughness of biogenic calcite secreted by the giant barnacle Austromegabalanus psittacus

“…A previous attempt with XRD and infrared spectroscopy did not reveal any significant amount of ACC in the balanid Balanus amphitrite 50 . Our calculation is well below previous estimations for other biogenic calcites: the sea urchin test plates and spines (~ 10% ACC) with similar methods 56 , sea urchin spines (~ 8 at.%) with 11 C nuclear magnetic resonance (NMR) 11 , and bivalve calcite (~ 6.9 at.%) with X-ray absorption near edge structure (XANES) 57 . From DSC curves, heat flow peaks associated with organic matter combustion from 290 °C to 500 °C and carbonate thermal decomposition from 600 to 900 °C were detected ( Supplementary Fig.…”

“…Determination of ACC by X-ray diffraction (XRD) and thermogravimetric analysis (TGA)-differential scanning calorimetry (DSC). Following the methodology described by Albéric et al 56 , we combined XRD, TGA, and DSC to determine the wt% of ACC. XRD scan of the mixture of shell material and silicon (20%) as internal standard was used to determine the percentage of amorphous material using the Rietveld refinement method ( Supplementary Fig.…”

On the Relation of Amorphous Calcium Carbonate and the Macromechanical Properties of Sea Urchin Spines

“…[7] This mesocrystal structure contains between 8 and 10 wt% ACC in mature spines. [7,12] Although the influence of the organic macromolecules on the fracture and micromechanical properties of sea urchin spines is well studied, it has not been investigated yet, how their macromechanical properties, such as compressive strength, bending strength, and Young's modulus are affected by the ACC content. This study sets out to fill this gap.…”

Automatic Crack Detection and Analysis for Biological Cellular Materials in X-Ray In Situ Tomography Measurements

“…Compared to the fully organic (e.g., wood, cork, porcupine quill, etc.) and partially mineralized (e.g., trabecular bone) biological cellular materials, the porous microstructure of echinoderm skeletal elements represents a unique class of biological ceramic cellular materials due to its high mineral density (> 98.4 wt%) [3] and excellent damage tolerance [4][5][6]. This is in stark contrast to many synthetic ceramic cellular solids, which often exhibit immediate structural degradation when loading exceeds the structure's strength, leading to limited energy absorption capabilities [7][8][9].…”