Organic membranes determine the pattern of the columnar prismatic layer of mollusc shells

Abstract

The degree to which biological control is exercised compared to physical control of the organization of biogenic materials is a central theme in biomineralization. We show that the outlines of biogenic calcite domains with organic membranes are always of simple geometries, while without they are much more complex. Moreover, the mineral prisms enclosed within the organic membranes are frequently polycrystalline. In the prismatic layer of the mollusc shell, organic membranes display a dynamics in accordance with the von Neumann-Mullins and Lewis Laws for two-dimensional foam, emulsion and grain growth. Taken together with the facts that we found instances in which the crystals do not obey such laws, and that the same organic membrane pattern can be found even without the mineral infilling, our work indicates that it is the membranes, not the mineral prisms, that control the pattern, and the mineral enclosed within the organic membranes passively adjusts to the dynamics dictated by the latter.

Physical and Biological Determinants of the Fabrication of Molluscan Shell Microstructures

“…Mollusc shells are organo-mineral biocomposites, in which the mineral part constitutes 95-99% of the shell weight while the organic fraction makes up 0.1-5% (Hare and Abelson, 1965). Exceptional values of up to 16% organic matter have been recorded in the calcitic columnar prismatic layers of the pteriomorph bivalve Pinna nobilis (Checa et al, 2016a). Despite its small volumetric representation, the organic fraction is extremely complex, with hundreds of proteins, polysaccharides and lipids, which can differ according to molluscan group.…”

Macro-to-nano scale investigation of wall-plate joints in the acorn barnacle Semibalanus balanoides: correlative imaging, biological form and function, and bioinspiration

“…Elongated crystals in Semibalanus alae have previously been identified from a single study of B. balanus and S. balanoides [17] that was limited to two dimensional study (LM and SEM) and left their origins unexplained, and elongate crystals have been identified in B. amphitrite [19,21]. Different crystallographic orientations, in particular elongate, prismatic columns associated with organic materials are common in a variety of biomineralised molluscs [6,42,43] but remain largely unidentified in barnacles. The ordering of calcite in the scutum (one of the two plates that guard the apical opercular opening) is significantly disordered compared with the calcite in the wall-plates in A. amphitrite [19], and the calcitic microcrystals in the wall plates of this species show almost no orientation [19,21] whilst those in the base plate of A. amphitrite shows some preferred alignment [21].…”

“…The involvement of organic material in the biomineralisation of specific crystal structures and orientations could have a bearing on the function of the ala pores, and may represent channels/canals which hold or deliver biomineralisation products to specific areas of the exoskeleton. Organic membranes are known to influence the pattern of columnar prismatic layers in numerous mollusc shells [43], so it is possible that organic channels (or, ala pores) running through the barnacle structure contribute towards the delivery of and biomineralisation of calcium carbonate. The organic layer separating the ala tip and neighbouring plate may play a part in this.…”

Mineralization and non-ideality: on nature’s foundry

“…A prime example, from mollusk shells, is an inter-lamellar membrane composed of hydrophobic β-chitin and biomolecules. This matrix provides spatially periodic sites for crystallization and imparts a hierarchical organization to the growing mineral (Addadi et al 2003;Checa et al 2016;Nakahara 1991;Pereira-Mouriès et al 2002). 4.…”