Structural Control of Crystal Nuclei by an Eggshell Protein

Abstract

The use of biomolecules in nature to direct crystal growth leads to a degree of polymorph and morphology control that far surpasses anything currently accessible in a laboratory. Examples include the intricate nano-and microcrystalline structures found in mollusk shells, [1] coccoliths, [2] and eggshells, [3] which imbue the shells with important physical properties. Recent work has exploited biomolecules [4,5] and biomimetic processes [6,7] to fabricate new materials, but the scope for this would be greatly enhanced if the mechanism by which the biomolecules effect this control were better understood. Molecular simulation should be an ideal tool for identifying these mechanisms. Methods have been developed to model the clustering of inorganic ions on biomolecules, [8] but simulating the onset of long-range crystalline order in the inorganic deposit due to the biomolecule has not been possible. Crystal nucleation, a crucial step in polymorph selection, occurs on timescales that have hitherto been inaccessible to molecular simulation. Herein, we show that our recent developments to metadynamics, [9,10] coupled with the latest generation of leadership-class computing, have now made it possible to simulate the role of a native protein in controlling the onset of mineral crystallization. We illustrate this process with the first molecular simulation of spontaneous crystallization of amorphous CaCO 3 in the presence of the chicken eggshell protein ovocleidin-17 (OC-17).Eggshells have an intricate structure that consists of two domains attached to an inner membrane. [11] The first domain is an array of small polycrystalline calcite clusters (mammillary caps) attached to the membrane that surrounds the albumin; the second domain (pallisade layer) consists of elongated calcite crystals with partial alignment. Experiments have identified various proteins associated with eggshell formation. One class, C-type lectin-type proteins, is found only within the mineral region and is important in controlling calcite deposition. [12] In vitro studies with OC-17 (chicken) and ansocalcin (goose) have shown that these proteins promote calcite formation and define the crystal morphology. [13][14][15] There is now much experimental evidence that many biominerals, [16] including eggshells, [17] begin as nanoparticle deposits of an amorphous inorganic material. Our recent simulations [10] support this, showing amorphous calcium carbonate (ACC) to be energetically stable, even at larger particle sizes where calcite becomes thermodynamically preferred. The interaction between OC-17 and ACC particles of various sizes is therefore likely to be fundamental to the mechanism by which OC-17 controls calcite growth, and so forms the focus of the work described herein.Simulations [18] were performed using metadynamics (metaD). [19,20] MetaD extends conventional molecular dynamics (MD) to sample the free-energy landscape in terms of collective coordinates (that is, order parameters or reaction coordinates). It is particularly good at finding the rar...

Molecular dynamics simulation of protein-mediated biomineralization of amorphous calcium carbonate

“…[13][14][15] A recent study on the formation of coral skeleton demonstrated that the ACC phase is indeed the metastable precursor to the crystalline CaCO 3 , and that the growth rate of aragonite crystals through the non-classical crystallization process 11,12 involving aggregation of ACC particles is $100 times faster than the classical route of ion-by-ion formation of crystals. 16 Earlier studies have also shown that the binding affinity of Ovocleidin-17 (OC-17), a hen eggshell protein, for ACC nanoparticles is much higher than that for the calcite surface 17,18 suggesting that favorable binding of the protein to ACC is critical for biomineralization and eggshell formation. The lower calcite-protein binding affinity is leveraged for the detachment of the protein from the crystal aer the ACC to crystal transition.…”

“…The lower calcite-protein binding affinity is leveraged for the detachment of the protein from the crystal aer the ACC to crystal transition. 18 Thus, OC-17 or a class of functionally similar proteins/biopolymers can be regarded as catalysts to facilitate the crystallization of CaCO 3 .…”

Biomacromolecules enabled dendrite-free lithium metal battery and its origin revealed by cryo-electron microscopy

“…Biomineralization is a widespread phenomenon in nature leading to the formation of hierarchically structured minerals by living organisms [31][32][33] . It has been revealed that biomolecules, particularly the stereochemical side chains within them, can guide the nucleation and growth of mineral crystals [34][35][36][37] . As a well-known example in biomineralization, the eggshell has attracted much attention, because its calcified crystallization ( Fig.…”

Peptide-Polymer Conjugates as Model Systems To Explore the Functional Space of Precision Polymers

“…Bioinspired peptide-polymer/ protein-polymer conjugates are widely used for a broad range of applications (25), including enzyme stabilization (26)(27)(28)(29) the self-organization of bioconjugates (30)(31)(32)(33), or in adhesive systems, where proteins have proved to serve as excellent interfaces between organic and inorganic materials (34)(35)(36).…”