Spiral and target patterns in bivalve nacre manifest a natural excitable medium from layer growth of a biological liquid crystal

Abstract

Nacre is an exquisitely structured biocomposite of the calcium carbonate mineral aragonite with small amounts of proteins and the polysaccharide chitin. For many years, it has been the subject of research, not just because of its beauty, but also to discover how nature can produce such a superior product with excellent mechanical properties from such relatively weak raw materials. Four decades ago, Wada [Wada K (1966) Spiral growth of nacre. Nature 211:1427] proposed that the spiral patterns in nacre could be explained by using the theory Frank [Frank F (1949) The influence of dislocations on crystal growth. Discuss Faraday Soc 5:48 -54] had put forward of the growth of crystals by means of screw dislocations. Frank's mechanism of crystal growth has been amply confirmed by experimental observations of screw dislocations in crystals, but it is a growth mechanism for a single crystal, with growth fronts of molecules. However, the growth fronts composed of many tablets of crystalline aragonite visible in micrographs of nacre are not a molecular-scale but a mesoscale phenomenon, so it has not been evident how the Frank mechanism might be of relevance. Here, we demonstrate that nacre growth is organized around a liquid-crystal core of chitin crystallites, a skeleton that the other components of nacre subsequently flesh out in a process of hierarchical self-assembly. We establish that spiral and target patterns can arise in a liquid crystal formed layer by layer through the Burton-Cabrera-Frank [Burton W, Cabrera N, Frank F (1951) The growth of crystals and the equilibrium structure of their surfaces. Philos Trans R Soc London Ser A 243:299 -358] dynamics, and furthermore that this layer growth mechanism is an instance of an important class of physical systems termed excitable media. Artificial liquid crystals grown in this way may have many technological applications.biomineralization ͉ chitin ͉ interlamellar membranes ͉ mollusc T he splendor of a pearl extends even to under a microscope; with magnification, one can see that the nacreous surfaces of bivalve mollusks-clams, mussels, oysters, scallops, and so onare made up of a striking arrangement of spiral, target, and labyrinthine patterns (1); see Fig. 1. Nacre, or mother of pearl, is the iridescent material that forms an inner layer of the shells of numerous species of mollusks as well as the pearls that many of those same species produce. The structure of nacre is often likened to a brick wall, and indeed, it is composed of bricks of aragonite tablets (Ϸ95%) and mortar of organic so-called interlamellar membranes (polysaccharide and protein, Ϸ5%), but it is a brick wall built in a peculiar fashion, because first, the mortar is put in place, and then the bricks grow within it. (See Fig. 2 for a sketch of bivalve molluscan anatomy and nacre structure.) From an examination of the extrapallial space of the bivalve mollusk, the narrow liquid-filled cavity between the soft tissues and the shell of the organism, it is seen that the first visible feature in nacre growth ...

Physical and Biological Determinants of the Fabrication of Molluscan Shell Microstructures

“…Screw dislocations manifest themselves as the spiral patterns typically observed in the nacre of bivalves (Figure 7L) and gastropods, which are resolved at their very axis in a single tablet with screw growth (Figure 7L, inset). Spiral and target patterns have been modeled theoretically by assuming that the nacre formation system is an excitable medium, which conforms to a layer-bylayer liquid crystal (Cartwright et al, 2009). Bivalve nacre forms target patterns (Figure 7M), which are comparable to growth hillocks produced during the formation of new atom planes in a growing crystal.…”

Mineral bridges in nacre

“…It has a brick and mortar structure, in which the bricks are aragonite tablets (5-15 lm wide) and the mortar is composed of organic material (proteins and polysaccharides). Its secretion is fully extracellular and begins with the production of very closely spaced (100 nm) parallel interlamellar membranes (Nakahara, 1983(Nakahara, , 1991 through liquid crystallization (Cartwright and Checa, 2007;Cartwright et al, 2009). These consist of a core of b-chitin that is surrounded by acidic proteins (Levi-Kalisman et al, 2001).…”

Crystal growth as an excitable medium

“…Here, we show with a coupled map lattice model that the classical BCF model of crystal growth is also an excitable medium. As well as tangential growth of a solid crystal, we demonstrate that the excitable paradigm holds and the BCF model may be applied to layer-by-layer growth of a liquid crystal, which has recently been noted in the biomaterial nacre (or mother of pearl) [9].…”