Physical and Biological Determinants of the Fabrication of Molluscan Shell Microstructures

Abstract

Molluscs are grand masters in the fabrication of shells, because these are composed of the largest variety of microstructures found among invertebrates. Molluscan microstructures are highly ordered aggregates of either calcite or aragonite crystals with varied morphologies and three-dimensional arrangements. Classically, every aspect of the fabrication of microstructural aggregates is attributed to the action of proteins. There was, however, only direct evidence that the mineral phase, and indirect evidence that nucleation and the crystal shape, are determined by the types of soluble proteins. Some authors imply that crystal competition may also play a role. In addition, the fabrication of intergranular organic matrices typical of some microstructures (nacre, columnar prismatic) cannot have a protein-based explanation. Over the last decade I and collaborators have been applying a holistic view, based on analyzing and interpreting the features of both the organic (mantle, extrapallial space, periostracum, organic matrices) and inorganic (crystallite morphology, arrangement, and crystallography) components of the biomineralization system. By interpreting them on biophysical principles, we have accumulated evidence that, in addition to the activity of proteins, other mechanisms contribute in an essential way to the organization of molluscan microstructures. In particular, we have identified processes such as: (1) crystal nucleation on preformed membranes, (2) nucleation and growth of crystals between and within self-organized membranes, (3) active subcellular processes of contact recognition and deposition. In summary, besides the activity of organic macromolecules, physical (crystal competition, self-organization) and/or biological (direct cellular activity) processes may operate in the fabrication of microstructures. The balance between the physical and biological determinants varies among microstructures, with some being based exclusively on either physical or biological processes, and others having a mixed nature. Other calcifying invertebrates (e.g., corals, cirripeds, serpulids) secrete microstructures that are very similar to inorganic crystal aggregates, and only some brachiopods and, to a lesser extent, bryozoans may have secretory abilities comparable to those of molluscs. Here I provide a new perspective, which may allow microstructures to be understood in terms of evolutionary constraints, to compare the secretional abilities among taxa, and even to evaluate the probability of mimicking microstructures for the production of functional synthetic materials.

The Biomineralization Proteome: Protein Complexity for a Complex Bioceramic Assembly Process

“…The transcriptome or RNA expression levels in these organisms are also being explored with the goal of understanding the timing of transcription, translation, and protein secretion as it pertains to the events occurring in the biomineralizing matrix . What has emerged from these studies…”

“…The mollusk, of the phyla Lophotrochozoa, is one of the most diverse groups on Earth (>50 000 species) that creates a protective outer shell that has a high degree of organization, much more so than bone, and this system has been intensely studied for several decades . In most bivalve mollusks, the shell consists of three layers (Figure ): 1) the periostracum, which is a thin organic coating or “skin” comprising the outermost layer of the shell; 2) the prismatic layer, the outermost mineral layer of the shell that comprises organized parallel rods of single crystal calcite, a calcium carbonate polymorph; 3) nacre layer, or the innermost mineral layer of the shell that comprises hexagonal tablets of single crystal aragonite, a calcium carbonate polymorph, that are arranged in a “brick‐and‐mortar” organization . Both the prismatic and nacre mineral particles are coated with a protein‐containing film or layer that is termed the framework layer and this will be discussed in more detail below .…”

Microstructure and crystallography of the wall plates of the giant barnacleAustromegabalanus psittacus: a material organized by crystal growth

“…Accordingly, the corresponding extrapallial space must be relatively wide and variable in thickness. This is unlike bivalves [18] and rhynchonelliform brachiopods [19], in which some microstructures are produced across extremely thin (100 nm or less) extrapallial spaces. Accordingly, the crystals can protrude only by a matter of tens of nanometres.…”

“…In barnacles, the activity of the mantle cells seems restricted to delivering the necessary ingredients for crystal growth (calcium and carbonate ions, or amorphous calcium carbonate nanoaggregates) to the extrapallial space. This is again unlike other calcifiers, like molluscs or brachiopods, which are able to fabricate very sophisticated microstructures through a mixture of physical (self-organization processes) and biological (differential subcellular secretion, cellular contact recognition) processes [18]. Accordingly, the microstructural differences between barnacles and molluscs/brachiopods can be traced back to the secretory abilities of their mantles.…”

Growth of Nacre Biocrystals by Self-Assembly of Aragonite Nanoparticles with Novel Subhedral Morphology

“…(3) OBBs are probably initially formed in an extrapallial space with a thickness of ca. 100 nm [38], which implies that they should be <100 nm in size. Therefore, we predict that OBBs forming the SANs should be <100 nm in size.…”