1. Biomimetics: Learning From Nature for Novel Material Concepts Albert Yu-Min Lin, Po-Yu Chen, Marc A. Meyers Materials Science and Engineering Program University of California, San Diego, La Jolla, CA 92093-0411 Motivation: Crystallization of inorganic materials in nature generally occurs in ambient temperatures and pressures under isothermal, and isobaric conditions. Yet the simple organisms, through which these inorganic materials form, are able to create extremely precise and complex structures. Understanding the process in which living organisms control the growth of structured inorganic materials could lead to significant advances in material science, opening the door to novel synthesis techniques for nano-scale composites. Studying the growth process and structure of Abalone Shells: Both red (Haliotis rufescens) and green (Haliotis fulgens) abalone were raised in an controlled open water facility at the Scripps Institute of Oceanography, California. Culturing: 10 mm 5µm The “flat Pearl” method pioneered by the UC Santa Barbra group [1] was used to grow samples of nacre which could be extracted over varying time periods. This provides a time sequential model of nacre self-assembly from initial deposition to steady state growth. “Christmas tree” structure consisting of micron sized aragonite tiles separated by nanoscaled organic membranes. Flat Pearl: Self-Assembly: Under normal pressures and temperatures nature creates nanonscaled, hierarchical, composites with remarkable properties through a process of self- assembly. This involves the identification and manipulation of elements and ionic molecules from the local environment and their incorporation into functional structures through strict biological mediation [2]. Activation Energy Cascade for Minerals [3] Morphology: Understanding the crystallization path of biological materials is the key to understanding their mechanisms of self-organization. Nature does not have the ability to use the crystal growth techniques of modern laboratories, such as cooling high temperature melts. Yet nature’s composites are often found to have higher structural organization and control then any man made materials. How is this done? Kinetic favorability of each polymorphs is influenced by genetic, metabolic, and environmental processes Effect of organic matrix much larger for “B” then for “A”, “B” is kinetically favorable Both polymorphs are affected equally, “A” remains kinetically favorable Structure of typical mollusk shell is depicted above [5]. Both the external layer (prismatic calcite) and the internal region (aragonite) are shown. The mantle epithelium of the abalone is responsible for secreting the proteins that mediate shell growth. It ejects them to the extrapallial space. Small terrace cones are shown on the growth surface and correspond to the “Christmas tress” (a) Schematic representation of stacked layers of hexagonal aragonite tiles growing in the c- direction. (b) SEM image on fracture surface shows highly-ordered arrangement of tiles with consistent 0.5μm thickness and 10μm diameter. Micro and Macro Structure of Nacre: Nacre – A Composite: The shell is composed of 95% inorganic phase separated by thin organic sheets in a “brick and mortar” like system. Microstructure: 2µm2µm Inorganic Component – “Brick-like” hexagonal tiles of crystalline aragonite (an orthorhombic polymorph of CaCO3) form the organized micro-layers of nacre. There is a high degree of crystallographic texture characterized by nearly perfect “C-axis” alignment normal to the plane of the tiles. The macro scale structure reveals additional morphologies of the aragonite polymorph such as block-like and spherulitic. Organic Component – individual layers of aragonite tiles are separated by ~30nm protein sheets which act as the binding glue of the structure. The organic glue is believed to contain ridged beta sheets of proteins, however the identification of those proteins and the confirmation of this theory have not yet been fully completed. Macrostructure (mesolayers): (a) Random nucleation of aragonite crystals on protein. (b) Protein deposition causing the arrest of crystallographic growth in the “c” direction. (c) Enriched second growth spurt after deposition of beta sheet and nucleation. (d) First aragonite plates are butted together while growth of second layer continues in a direction. (e) Nucleation of third layer as second layer growth continues in a direction. Arrest of growth on c- axis, continued by random deposition of nucleation sites. Mineral Bridges continue growth through thin organic layers, allowing the transfer of crystal orientation Growth Mechanism Hypothesis: Organic involvement in nucleation morphology: It is believed that the biological strategy is to first nucleate a solid deposit which could be disordered and often hydrated, then transform that into a stable crystalline deposit over time. This would be done through a series of transient precursor phases [5]. However for the case of nacre, amorphous calcium carbonate is inherently unstable. The proteins which compose the thin layers of organic glue seem to induce the formation of stable amorphous calcium carbonate under nearly physiological pH and temperature conditions [6]. LEFT: Representatio n of activation energies of nucleation in the presence and absence of an organic matrix for two nonspecific polymorphs [4]. References [1] M. Fritz, A.M. Belcher, D.A. Walters, P.K. Hansma, G.D. Stucky, D.E. Morse, Nature 49 (1994) 371. [2] M. Sarikaya, Mater. Res. Soc. 174 (1990) 109. [3] S. Mann, Biomineralization. Oxford University Press. New York, (2001) 60. [4] S. Mann et. al, Science, 261 (1993) 1286. [5] S. Weiner, I. Sagi, L. Addadi, IScience I309, (2005) 1027. [6] J. Aizenberg, G. Lambert, L.Addadi, S. Weiner, Adv. Mater. 8, (1996) 222. [7] R. Menig, M.H. Meyers, M.A. Meyers, K.S. Vecchio, Acta Materialia 48, (2001) 2383. Parallel σ = 240 MPa Perpendicular σ = 550 MPa Compressive strength: Weibull statsitical analysis Fracture Mechanism Fracture surfaces after plastic deformation under tension. Under tensile stress, tiles of calcium carbonate can slide, absorbing energy. Because of this microstructure, the abalone shell can absorb a great deal of energy without failing. Conclusions 1.The growth proceeds by the sequential deposition of aragonite and organic layer along the c-axis orientation. The Christmas tree pattern was confirmed and an analytical model for growth is proposed. 2.The organic layer attaches itself to the basal planes of aragonite, so that there is virtually no organic material where platelets abut. This is consistent with the stereoselective attachment of proteins to the basal planes. 3.It is proposed that the animal injects, periodically, the organic material that arrests the growth in the c direction. If this growth were not arrested, long needles would form thatwould penetrate the extrapallial space and cause trauma to the epithelium. Based on this, a simple mechanism for growth is proposed. 4.Growth of aragonite is periodically arrested in abalone. Mesolayers of organic material with the thickness of approximately 10–20 μm are periodically formed as a result of seasonal fluctuations.They play a prominent role in the mechanical strength and are a determining factor in plastic microbuckling. 5.A mechanism for tensile deformation of the abalone is proposed, based on viscoplastic shear of the organic layer. Mechanical Properties: The advantage of composite structures in nature Inorganic materials are usually very weak and brittle. However, when combined with proteins, self-organized into highly ordered structures, these materials become very strong composites, increasing their strength by orders of magnitude. Abalone shell is one of the examples. We know that calcium carbonate, or chalk, is weak and brittle, yet the abalone shell consisting mainly of calcium carbonate shows excellent mechanical properties. Key to the strength of the shell is a positively charged protein adhesive that binds to the negatively charged top and bottom surfaces of the calcium carbonate tiles. The glue is strong enough to hold layers of tiles firmly together, but weak enough to permit the layers to slip apart, absorbing the energy of a heavy blow in the process. Schematic drawing of stacking of abalone tiles and their separation under tension. SEM photography after plastic deformation under tension; notice that fracture by tile “pullout”. Plot showing distribution of step lengths. Compression Test Samples of abalone shell were tested in compression both parallel and perpendicular to shell growth bands under quasi-static and dynamic strain rates. The directions of loading with respect to growth plane directions are presented in figure below. 10µm 2µm 10µm Week: 1 Week: 2 Week: 3 Week: 4 Week: 5 Week: 6 Macrostructure (mesolayers): Another type of structure is mesolayers (growth bands), which are approximately 300μm thick and separated by viscoplastic protein layer with a thickness about 20 μm. The SEM photograph shows two dark layers of protein. The inside of the shell is in the bottom. The upper surface of the organic layer is smooth, block-like aragonite, while its lower surface is irregular, spherulitic aragonite. Environmental dependence of shell growth: Mesolayers (growth bands) correspond to periodic growth arrest. Phase transformations occurs due to environmental changes in seawater. Optical micrograph showing macrostructure with 0.3mm inorganic layers separate by 20μm protein layers. Tiled aragonite growth Block-like aragonite growth Protein layers without mineral growth Spherulitic aragonite growth SEM micrograph showing three morphologies of aragonite. Growth direction Sequential Growth of Abalone Shells The plate-pearl method is used to study the detail of growth process. Six mature red abalones were inserted with 8-10 glass slides. The glass slides were then pulled out every week and observed under environmental SEM in Scripps Institute of Oceanography. The continuous growth morphology of abalone shell from the first to sixth week is shown in the flow chart. After six weeks, the shell growth reach steady state with sophisticated “Christmas tree” structue. Schematic diagram showing pull-out of overlapping tile layers: (a) three-dimensional view (b) two-dimensional view (c) Force diagram Toughness enhanced by mesolayers The mesolayers (growth bands) play an important role in damage control and mechanical strength. The organic protein layers create parallel viscoplastic deforamtion under shear stress, and plastic microbuckling (kinking) under compressive loading. The mechanisms are observed under SEM by Menig et al.[7] Microbuckling observed in compression testing of abalone specimens (a)Viscoplastic deformatiom (b)Crack deflection (c)Plastic micobuckling (kinking) Applications: