Peter Fratzl

Materials become insensitive to flaws at nanoscale: Lessons from nature

Natural materials such as bone, tooth, and nacre are nanocomposites of proteins and minerals with superior strength. Why is the nanometer scale so important to such materials? Can we learn from this to produce superior nanomaterials in the laboratory? These questions motivate the present study where we show that the nanocomposites in nature exhibit a generic mechanical structure in which the nanometer size of mineral particles is selected to ensure optimum strength and maximum tolerance of flaws (robustness). We further show that the widely used engineering concept of stress concentration at flaws is no longer valid for nanomaterial design.

Structure and mechanical quality of the collagen–mineral nano-composite in bone

Bone is a hierarchically structured material with remarkable mechanical performance which may serve as a model for the development of biomimetic materials. Understanding its properties is essential for the assessment of diseases such as osteoporosis. This will lead to a critical evaluation of current therapies and aid in their more targeted development. While the full hierarchical structure of bone is extremely complex and variable, its basic building block, the mineralized collagen fibril, is rather universal. Due to the progress in experimental methods to characterize materials at the nanoscale, new insights have been gained into the structure/mechanical function relation in this nanocomposite. The amount of mineral is usually thought to determine the stiffness of the material, but recent results suggest that the properties of the organic matrix as well as the geometrical arrangement of the two components might have a much larger influence on the properties than traditionally assumed. Some recent results from experiment and numerical modeling leading to these ideas are reviewed.

Cooperative deformation of mineral and collagen in bone at the nanoscale

In biomineralized tissues such as bone, the recurring structural motif at the supramolecular level is an anisotropic stiff inorganic component reinforcing the soft organic matrix. The high toughness and defect tolerance of natural biomineralized composites is believed to arise from these nanometer scale structural motifs. Specifically, load transfer in bone has been proposed to occur by a transfer of tensile strains between the stiff inorganic (mineral apatite) particles via shearing in the intervening soft organic (collagen) layers. This raises the question as to how and to what extent do the mineral particles and fibrils deform concurrently in response to tissue deformation. Here we show that both mineral nanoparticles and the enclosing mineralized fibril deform initially elastically, but to different degrees. Using in situ tensile testing with combined high brilliance synchrotron X-ray diffraction and scattering on the same sample, we show that tissue, fibrils, and mineral particles take up successively lower levels of strain, in a ratio of 12:5:2. The maximum strain seen in mineral nanoparticles (≈0.15–0.20%) can reach up to twice the fracture strain calculated for bulk apatite. The results are consistent with a staggered model of load transfer in bone matrix, exemplifying the hierarchical nature of bone deformation. We believe this process results in a mechanism of fibril–matrix decoupling for protecting the brittle mineral phase in bone, while effectively redistributing the strain energy within the bone tissue.

Iron-Clad Fibers: A Metal-Based Biological Strategy for Hard Flexible Coatings

Mussel Fibers While it is possible to make strong fibers or threads from organic materials, most suffer from high wear abrasion. Marine mussels attach themselves to rocky seashores using a series of byssal threads. Despite the constant rubbing caused by the motion of the tides, the threads show high wear resistance. Harrington et al. (p. 216, published online 4 March; see the Perspective by Messersmith) now find that the threads are protected by a proteinaceous outer cuticle that is rich in the amino acid 3,4-dihydroxyphenylalanine (dopa), which is known to be a strong adhesive. The cuticle is also rich in metal ions, primarily Fe3+. The dopa-metal crosslinks helped to form the tough outer coating. Marine mussel byssal threads have an outer coating in which proteins are linked to metal ions. The extensible byssal threads of marine mussels are shielded from abrasion in wave-swept habitats by an outer cuticle that is largely proteinaceous and approximately fivefold harder than the thread core. Threads from several species exhibit granular cuticles containing a protein that is rich in the catecholic amino acid 3,4-dihydroxyphenylalanine (dopa) as well as inorganic ions, notably Fe3+. Granular cuticles exhibit a remarkable combination of high hardness and high extensibility. We explored byssus cuticle chemistry by means of in situ resonance Raman spectroscopy and demonstrated that the cuticle is a polymeric scaffold stabilized by catecholato-iron chelate complexes having an unusual clustered distribution. Consistent with byssal cuticle chemistry and mechanics, we present a model in which dense cross-linking in the granules provides hardness, whereas the less cross-linked matrix provides extensibility.

Biomimetic materials research: what can we really learn from nature's structural materials?

Nature provides a wide range of materials with different functions and which may serve as a source of bio-inspiration for the materials scientist. The article takes the point of view that a successful translation of these ideas into the technical world requires more than the observation of nature. A thorough analysis of structure-function relations in natural tissues must precede the engineering of new bio-inspired materials. There are, indeed, many opportunities for lessons from the biological world: on growth and functional adaptation, about hierarchical structuring, on damage repair and self-healing. Biomimetic materials research is becoming a rapidly growing and enormously promising field. Serendipitous discovery from the observation of nature will be gradually replaced by a systematic approach involving the study of natural tissues in materials laboratories, the application of engineering principles to the further development of bio-inspired ideas and the generation of specific databases.

Biomaterial systems for mechanosensing and actuation.

Living organisms use composite materials for various functions, such as mechanical support, protection, motility and the sensing of signals. Although the individual components of these materials may have poor mechanical qualities, they form composites of polymers and minerals with a remarkable variety of functional properties. Researchers are now using these natural systems as models for artificial mechanosensors and actuators, through studying both natural structures and their interactions with the environment. In addition to inspiring the design of new materials, analysis of natural structures on this basis can provide insight into evolutionary constraints on structure–function relationships in living organisms and the variety of structural solutions that emerged from these constraints.

Nucleation and growth of magnetite from solution

The formation of crystalline materials from solution is usually described by the nucleation and growth theory, where atoms or molecules are assumed to assemble directly from solution. For numerous systems, the formation of the thermodynamically stable crystalline phase is additionally preceded by metastable intermediates . More complex pathways have recently been proposed, such as aggregational processes of nanoparticle precursors or pre-nucleation clusters, which seem to contradict the classical theory. Here we show by cryogenic transmission electron microscopy that the nucleation and growth of magnetite-a magnetic iron oxide with numerous bio- and nanotechnological applications-proceed through rapid agglomeration of nanometric primary particles and that in contrast to the nucleation of other minerals, no intermediate amorphous bulk precursor phase is involved. We also demonstrate that these observations can be described within the framework of classical nucleation theory.

Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays

The continuously forming fin bony rays of zebrafish represent a simple bone model system in which mineralization is temporally and spatially resolved. The mineralized collagen fibrils of the fin bones are identical in structure to those found in all known bone materials. We study the continuous mineralization process within the tissue by using synchrotron microbeam x-ray diffraction and small-angle scattering, combined with cryo-scanning electron microscopy. The former provides information on the mineral phase and the mineral particles size and shape, whereas the latter allows high-resolution imaging of native hydrated tissues. The integration of the two techniques demonstrates that new mineral is delivered and deposited as packages of amorphous calcium phosphate nanospheres, which transform into platelets of crystalline apatite within the collagen matrix.

RADIAL PACKING, ORDER, AND DISORDER IN COLLAGEN FIBRILS

Collagen fibrils resemble smectic, liquid crystals in being highly ordered axially but relatively disordered laterally. In some connective tissues, x-ray diffraction reveals three-dimensional crystallinity in the molecular packing within fibrils, although the continued presence of diffuse scatter indicates significant underlying disorder. In addition, several observations from electron microscopy suggest that the molecular packing is organized concentrically about the fibril core. In the present work, theoretical equatorial x-ray diffraction patterns for a number of models for collagen molecular packing are calculated and compared with the experimental data from tendon fibrils. None of the models suggested previously can account for both the crystalline Bragg peaks and the underlying diffuse scatter. In addition, models in which any of the nearest-neighbor, intermolecular vectors are perpendicular to the radial direction are inconsistent with the observed radial orientation of the principal approximately 4 nm Bragg spacing. Both multiple-start spiral and concentric ring models are devised in which one of the nearest-neighbor vectors is along the radial direction. These models are consistent with the radial orientation of the approximately 4 nm spacing, and energy minimization results in radially oriented crystalline domains separated by disordered grain boundaries. Theoretical x-ray diffraction patterns show a combination of sharp Bragg peaks and underlying diffuse scatter. Close agreement with the observed equatorial diffraction pattern is obtained. The concentric ring model is consistent with the observation that the diameters of collagen fibrils are restricted to discrete values.

The effect of geometry on three-dimensional tissue growth.

Tissue formation is determined by uncountable biochemical signals between cells; in addition, physical parameters have been shown to exhibit significant effects on the level of the single cell. Beyond the cell, however, there is still no quantitative understanding of how geometry affects tissue growth, which is of much significance for bone healing and tissue engineering. In this paper, it is shown that the local growth rate of tissue formed by osteoblasts is strongly influenced by the geometrical features of channels in an artificial three-dimensional matrix. Curvature-driven effects and mechanical forces within the tissue may explain the growth patterns as demonstrated by numerical simulation and confocal laser scanning microscopy. This implies that cells within the tissue surface are able to sense and react to radii of curvature much larger than the size of the cells themselves. This has important implications towards the understanding of bone remodelling and defect healing as well as towards scaffold design in bone tissue engineering.