Stephen Weiner

Design strategies in mineralized biological materials

Organisms have been producing mineralized skeletons for the past 550 million years. They have evolved many different strategies for improving these materials at almost all hierarchical levels from Angstroms to millimetres. Key components of biological materials are the macromolecules, which are intimately involved in controlling nucleation, growth, shaping and adapting mechanical properties of the mineral phase to function. One interesting tendency that we have noted is that organisms have developed several strategies to produce materials that have more isotropic properties. Much can still be learned from studying the principles of structure–function relations of biological materials. Some of this information may also provide new ideas for improved design of synthetic materials.

Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth

Sea urchin larvae form an endoskeleton composed of a pair of spicules. For more than a century it has been stated that each spicule comprises a single crystal of the CaCO3 mineral, calcite. We show that an additional mineral phase, amorphous calcium carbonate, is present in the sea urchin larval spicule, and that this inherently unstable mineral transforms into calcite with time. This observation significantly changes our concepts of mineral formation in this well–studied organism.

Bone structure: from angstroms to microns.

Bone has a complex hierarchical structure, which despite much investigation, is still not well, understood. Here we bring together pieces of this complicated puzzle, albeit from different sources, to present a tentative overview of bone structure. The basic building blocks are the extremely small plate‐shaped crystals of carbonate apatite, just hundreds of ångstroms long and wide and some 20–30 Å thick. They are arranged in parallel layers within the collagenous framework. At the next hierarchical level these mineral‐filled collagen fibrils are ordered into arrays in which the fibril axes and the crystal layers are all organized into a 3‐dimensional structure that makes up a single layer or lamella of bone a few microns thick. The orientations of the collagen fibrils and the crystal layers in alternating lamellae of rat bone differ such that in the thinner lamellae, the fibrils and the crystal layers are parallel to the lamellar boundaries. In the thicker lamellae the fibrils are parallel to the boundary, but the crystal layers are rotated out of the plane of the boundary. In many bones these alternating lamellae are organized into even larger ordered structures to produce what is truly a remarkably ordered material, all the way from the molecular scale to the macroscopic product.—Weiner, S.; Traub, W. Bone structure: from ångstroms to microns. FASEB J. 6: 879‐885; 1992.

States of preservation of bones from prehistoric sites in the Near East: A survey

Abstract A survey of the states of preservation of organic material in 30 fossil bones from 16 different prehistoric sites in the Near East shows that whereas almost all the bones have little or no collagen preserved, they do, with few exceptions, contain non-collagenous proteins. These macromolecules, therefore, represent an important reservoir of indigenous fossil bone constituents.

Biological Control of Crystal Texture: A Widespread Strategy for Adapting Crystal Properties to Function

Textures of calcite crystals from a variety of mineralized tissues belonging to organisms from four phyla were examined with high-resolution synchrotron x-ray radiation. Significant differences in coherence length and angular spread were observed between taxonomic groups. Crystals from polycrystalline skeletal ensembles were more perfect than those that function as single-crystal elements. Different anisotropic effects on crystal texture were observed for sea urchin and mollusk calcite crystals, whereas none was found for the foraminifer, Patellina, and the control calcite crystals. These results show that the manipulation of crystal texture in different organisms is under biological control and that crystal textures in some tissues are adapted to function. A better understanding of this apparently widespread biological phenomenon may provide new insights for improving synthetic crystal-containing materials.

Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation

A significant proportion of the soluble protein of the organic matrix of mollusk shells is composed of a repeating sequence of aspartic acid separated by either glycine or serine. This regularly spaced, negatively charged aspartic acid may function as a template upon which mineralization occurs.

Organization of hydroxyapatite crystals within collagen fibrils

Transmission electron micrographs of individual mineralized collagen fibrils show that hydroxyapatite crystals are located mainly within the fibrils at the level of the gap regions. The plate‐shaped crystals are observed to be more or less uniformly stacked across the fibril diameter. We therefore suggest that the crystals are primarily located in ‘grooves’ created by contiguous adjacent gaps. The proposal is consistent with the observed crystal distribution in the fibril and with their average widths, which are almost 10‐times greater than an individual gap diameter.

X‐ray diffraction study of the insoluble organic matrix of mollusk shells

Mollusk shells are generally composed of calcium carbonate in an organic matrix. The organic matrix is observed to form prior to mineralization [ 1,2], and it has been suggested that some of the matrix protein components may serve as a template for mineral deposition [3-61. The calcium carbonate of the shell can be dissolved in EDTA leaving an insoluble fraction which comprises the bulk of the organic matrix [5,7,8] and consists of a heterogeneous mixture of proteins and carbohydrate [9-l 21. X-ray diffraction patterns reported for various organic matrices [13-l 71 are quite poor in detail and, apart from suggestions that they may contain (Yand /3-keratin-type features [ 16,171, have not led to structural interpretations. We describe here a new X-ray fiber diffraction study of insoluble organic matrices of shells representing the three major classes of mollusks. This enabled us to establish that the ordered protein components in the insoluble fraction adopt an antiparallel P-sheet conformation and that, where recognizable, the polysaccharide phase is chitin. We have determined the structural parameters of these phases, and have also investigated the relative orientations of the protein, mineral crystals and, in some cases, the chitin for several shell layers.

Aspartic acid-rich proteins: major components of the soluble organic matrix of mollusk shells.

SummaryDEAE-cellulose ion-exchange chromatography separates soluble organic matrix components of three mollusk shells, each from a different taxonomic class, into analogous subfractions. The proteins of all subfractions are enriched in acidic and polar amino acids. In each chromatogram, however, the subfraction which contains the major portion of total protein also contains the highest concentration of aspartic acid. Thus the major components of the soluble organic matrix are aspartic acid-rich proteins. The identification of these proteins in mollusks, together with the known occurrence of aspartic acid and phosphoserine-rich proteins in vertebrate tooth dentin, emphasizes the fundamental importance of such acidic proteins in the processes of mineralization.

Acidic macromolecules of mineralized tissues : the controllers of crystal formation

The deposition of minerals within many biological tissues is a controlled process. Among the most active agents that control biological mineralization are a group of unusually acidic proteins and glycoproteins. These can interact specifically with some crystal faces but not others, induce oriented nucleation, or intercalate in a regular manner into the crystal lattice itself.