The systematic fabrication of advanced materials will require the construction of architectures over scales ranging from the molecular to the macroscopic. The basic constructional processes of biomineralization—supramolecular pre-organization, interfacial molecular recognition (templating) and cellular processing—can provide useful archetypes for molecular-scale building, or ‘molecular tectonics’, in inorganic materials chemistry.

Molecular tectonics in biomineralization and biomimetic materials chemistry

Biological materials: Functional adaptations and bioinspired designs

Many organisms construct structural ceramic (biomineral) composites from seemingly mundane materials; cell-mediated processes control both the nucleation and growth of mineral and the development of composite microarchitecture. Living systems fabricate biocomposites by: (i) confining biomineralization within specific subunit compartments; (ii) producing a specific mineral with defined crystal size and orientation; and (iii) packaging many incremental units together in a moving front process to form fully densified, macroscopic structures. By adapting biological principles, materials scientists are attempting to produce novel materials. To date, neither the elegance of the biomineral assembly mechanisms nor the intricate composite microarchitectures have been duplicated by nonbiological processing. However, substantial progress has been made in the understanding of how biomineralization occurs, and the first steps are now being taken to exploit the basic principles involved.

https://science.sciencemag.org/content/sci/255/5048/1098.full.pdf

Innovative materials processing strategies: a biomimetic approach

In the last few years, the field of molluscan biomineralization has known a tremendous mutation, regarding fundamental concepts on biomineralization regulation as well as regarding the methods of investigation. The most recent advances deal more particularly with the structure of shell biominerals at nanoscale and the identification of an increasing number of shell matrix protein components. Although the matrix is quantitatively a minor constituent in the shell of mollusks (less than 5% w/w), it is, however, the major component that controls different aspects of the shell formation processes: synthesis of transient amorphous minerals and evolution to crystalline phases, choice of the calcium carbonate polymorph (calcite vs aragonite), organization of crystallites in complex shell textures (microstructures). Until recently, the classical paradigm in molluscan shell biomineralization was to consider that the control of shell synthesis was performed primarily by two antagonistic mechanisms: crystal nucleation and growth inhibition. New concepts and emerging models try now to translate a more complex reality, which is remarkably illustrated by the wide variety of shell proteins, characterized since the mid-1990s, and described in this chapter. These proteins cover a broad spectrum of pI, from very acidic to very basic. The primary structure of a number of them is composed of different modules, suggesting that these proteins are multifunctional. Some of them exhibit enzymatic activities. Others may be involved in cell signaling. The oldness of shell proteins is discussed, in relation with the Cambrian appearance of the mollusks as a mineralizing phylum and with the Phanerozoic evolution of this group. Nowadays, the extracellular calcifying shell matrix appears as a whole integrated system, which regulates protein-mineral and protein-protein interactions as well as feedback interactions between the biominerals and the calcifying epithelium that synthesized them. Consequently, the molluscan shell matrix may be a source of bioactive molecules that would offer interesting perspectives in biomaterials and biomedical fields.

Molluscan shell proteins: primary structure, origin, and evolution.

Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using cryo-TEM.

An electron-microscopic study was made of nacreous shell growth in several species of marine molluscs. Studies of sections of mantle-shell preparations show that the first step in crystal formation is the “polymerization” of part of the pallial fluid to form lamellae parallel to the surface of the epithelium. These lamellae form compartments enclosing a modified apallial fluid. Initiation of crystals occurs in these compartments in contact with a crystal in an adjacent layer. During crystal growth the organic matrix present in the compartment is displaced by the growing surface of the crystal. When growth is complete the crystal is entirely enveloped by a delicate organic sheath. These studies show that the pallial fluid with its organic constituents is responsible for supplying a matrix or substrate for crystal initiation and growth. It serves as a regulatory device for guiding the orderly growth and arrangement of crystals and, further, it may participate in the induction of new crystals. The formation of compartments during shell growth accounts for the uniform thickness, preferred exhibited orientation and mineralogy of the crystals as well as other features exhibited by the mature nacre.

An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs.

Observations were conducted at the light and electron microscope level of the formation and mineralization of dentin. At the light level it was shown that predentin is made up of the odontoblast process, collagen fibers and a ground substance. As mineralization occurs, the fibers tend to condense and thicken in areas adjacent to the odontoblast process. Fibers continue to invade the developing matrix and, as in early dentinogenesis, they appear at all times to be derived from the pulp. At the E.M. level the significant observations made in reference to dentin formation consist of the identification of granular masses appearing in the interfibrillar spaces initially in the region of the dentino enamel junction. Histochemical tests at the E.M. level demonstrated that the odontoblasts elaborate an acid mucopolysaccharide which concentrates in granules at the base of the odontoblast process. Subsequently these granules are extruded into the matrix where the polysaccharide becomes concentrated in the interfibrillar spaces and to some extent on the collagen fibers. The onset of mineralization occurs in the patches of mucopolysaccharide, later also on the fibers. It appears that in the presence of an acid mucopolysaccharide is a prerequisite for mineralization in the dental matrix.

The formation and mineralization of dentin

The effect of tetracycline on mineralization and growth.

A dorsal and ventral gland composed of large, flask-shaped cells located in the margin of the mantle ofLittorina give rise to the inner and outer layers of the periostracum respectively. The material comprising the periostracum is derived from secretory granules elaborated by the Golgi apparatus. When the Golgi granules of the ventral gland which consist of a substance exhibiting a definite periodicity, are discharged at the surface in contact with sea water, they are widely dispersed and consist of particles embedded in a substrate. Formation of the outer periostracum involves the re-aggregation of the Golgi secretory particles into a dense sheet which exhibits a periodicity of 300 A. Viewed in transverse section the periostracum exhibits a lattice pattern suggestive of a crystalline substance. The outer layer eventually reaches a thickness of 4–5 μ. The inner layer is derived from the secretory granules of the dorsal gland. The formation of the inner layer occurs in a manner similar to that of the outer layer. It does not, however, exhibit a periodicity. In the mature state it attains a thickness of 0.4–0.5 μ. In addition to a protective function the periostracum provides a barrier between the sea water and the pallial space and also regulates the site and arrangement of mineral crystal formation at the growing margin of the shell.

An electron microscope study of the formation and structure of the periostracum of a gastropod,Littorina littorea

An electron microscope study was made of the formation and structure of the inner ligament ofMytilus edulis andPinctada radiata. This part of the ligament is derived from the isthmus cells which are irregular columnar in shape. They exhibit a prominent rough endoplasmic reticulum and a Golgi apparatus, which are concerned with the elaboration of vesicles and granules eventually incorporated into an integral part of the conchiolin.

Gerrit Bevelander

Papers

An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs.

The formation and mineralization of dentin

The effect of tetracycline on mineralization and growth.

An electron microscope study of the formation and structure of the periostracum of a gastropod,Littorina littorea

An electron microscope study of the formation of the ligament of Mytilus edulis and Pinctada radiata