Vanessa Schoeppler,a Robert Lemanis,a Elke Reich,a Tamás Pusztai,b László Gránásy,b,c Igor Zlotnikov a
a B CUBE–Center for Molecular Bioengineering, Technische Universität Dresden, 01307 Dresden, Germany
b Wigner Research Centre for Physics, P.O. Box 49, H-1525 Budapest, Hungary
c Brunel Centre of Advanced Solidification Technology, Brunel University, Uxbridge, Middlesex UB8 3PH, UK
Molluscan shells are regarded as a classic model system for studying the formation–structure–function relationships during biomineralization, a process that yields hierarchically structured organic-inorganic composite structures in living organisms. Typically, the mollusc shells consist of a number of highly mineralized ultrastructures of complex mineral–organic architecture. Remarkably, shells of mollusc species from different classes display similar ultrastructural motifs. These hierarchically organized biocomposites in many cases provide enhanced strength and toughness compared to the pure mineral phase and superiority compared to modern man-made composites.
In a recent article that appeared in the prestigious journal Proceeding of the National Academy of Sciences (US, impact factor: 9.58), scientists from the Wigner Research Centre for Physics (Hungary) and the Technical University Dresden (Germany) investigated a possible link between microstructures observed during directional solidification, well known in materials science, and rather similar structures that form during biomineralization. In this study, ultrastructural morphogenesis of shells from three major molluscan classes, a bivalve Unio pictorum, a cephalopod Nautilus pompilius, and a gastropod Haliotis asinine, is compared to phase-field simulations based on the concept of directional solidification. It is demonstrated that by regulating only the chemical and physical boundary conditions during directional solidification, phase-field modelling can capture the generic features of the molluscan ultrastuctures, including a granular layer of randomly oriented crystallites, a “prismatic” layer of columnar crystals, and a multilayered nacre or “mother of pearl” domain built of alternating organic and inorganic layers (see Fig. 1).
Based on these findings, an architectural constraint is proposed for the evolution of molluscan shells: the morphospace of possible shell ultrastructures is bounded by the thermodynamic and kinetic limitations of directional crystal growth.
The experiments were performed at the Technical University of Dresden, whereas the computer simulations were done at the Wigner Research Centre for Physics.
Fig. 1: Cross-sectional change of the shell microstructure (left) in the electron microscope image of the shell of Nautilus pompilius, and (right) the simulated microstructure predicted by the phase-field theory (different colours indicate different crystallographic orientations). Growth direction is upwards. Note the following sequence of morphological transitions in both panels: granular → columnar → nacre.
Animations: Computer animations that show the time evolution of the shell microstructure as predicted by phase-field modelling:
(a) Spatial distribution of the concentration c of calcium carbonate (the higher is c the yellower the colour, the mantle of the mollusc is black); (b) phase-field map (red is the extrapallial fluid between the mantle of the mollusc and solidification front, yellow stands for the calcium carbonate crystal, whereas the mantle is white); (c) orientation map (different colours correspond to different crystallographic orientations, the extrapallial fluid is black, and the mantle is white)
Link to the paper: https://www.pnas.org/content/116/41/20388.full
Press release of the Technical University Dresden: https://www.eurekalert.org/pub_releases/2019-09/tud-cgk092319.php
This work was supported by the "Frontline" excellence programme of the National Research, Development and Innovation Office (Hungary) under contract no. KKP-126749.