Biomimetics: materials fabrication through biology.

M multicellular organisms produce hard tissues such as bones, teeth, shells, skeletal units, and spicules (1). These hard tissues are biocomposites and incorporate both structural macromolecules (lipids, proteins, and polysaccharides) and minerals of, perhaps, 60 different kinds, including hydroxyapatite, calcium carbonate, and silica. A number of single-celled organisms (bacteria and algae) also produce inorganic materials either intracellularly or extracellularly (2). Examples include magnetotactic bacteria, which synthesize magnetite (3); chrysophytes (4), diatoms, and actinopoda (radiolarians; ref. 5), which synthesize siliceous materials; and S layer bacteria that have gypsum and calcium carbonate surface layers (6). Normally, hard tissues are mechanical devices (e.g., skeletal, cutting, grinding), or they serve a physical function (e.g., magnetic, optical, piezoelectric). Bioinorganics are also ion sources that are vital for physiological activities and, therefore, integral parts of the organisms (1, 2). Recently, a different single-celled organism has been added to the list of inorganic particle producers. Klaus et al. (7) have found that single crystalline silver-based particles of well defined compositions and shapes are synthesized by Pseudomonas stutzeri AG259, a bacterial strain previously isolated from a silver mine (8). The study reports on the detailed structure and phase composition of the silver-containing particles with a flat morphology that form within the periplasmic space. Currently, neither the synthesis mechanism nor the physiological nature of the particles is known. The presence of inorganic materials within organisms has broad implications in physical sciences, such as geology, mineralogy, physics, chemistry, and materials science (9, 10), as well as in biological fields, such as zoology, microbiology, morphology, physiology, evolution, and cellular biology (1, 2). The structures of biocomposites are highly controlled from the nanometer to the macroscopic levels, resulting in complex architectures that provide multifunctional properties. Therefore, there is much interest in inorganic material formation by organisms in these scientific fields (9–11). While biosciences are studying the implications of biomineralization in organismal physiology and its importance in species diversity and evolution, physical sciences focus on the mechanisms of formation and functional characteristics of inorganic materials. The synthesis mechanisms of inorganics by multicellular and single-celled organisms may be vastly different. Nonetheless, the presence of an inorganic compound in conjunction with a biological macromolecule within a tissue is intriguing in terms of the phase compatibility in these complex systems (9, 10). Furthermore, many aspects of composite materials biosynthesis are unusual from the traditional point of view of materials synthesis. These characteristics include the mineralogy of the inorganic; its phase composition, size, distribution, and morphology; its crystallography; its long-range orientational order of domains (texture); and its hierarchical organization. In multicellular organisms, bioinorganics are synthesized by a coordinated process involving cohort of similar cells, such as, in mammals, osteoblasts in bone (12) or dentinoblasts in dentin (13). Both of these hard tissues are extracellularly synthesized by these cells that control size, distribution, and morphology of the hydroxyapatite mineral particles (14). The resulting hard tissues are composites of particles within structural proteins (Fig. 1A). Dentin, enamel, and bone are known to be multifunctional, serving as loadbearing systems with piezoelectric properties. Similarly, in shell-forming molluscan species, mantel cells synthesize hard tissues that are differentiated into many different architectures. These include layered, columnar, and foliated structures of crystalline units that are allotropic forms of calcium carbonate (15). For example, in Haliotis rufescens, the gastropod commonly known as red abalone, columnar calcitic crystals constitute the prismatic section, whereas layered aragonitic platelets form the nacre (mother-of-pearl; Fig. 1B). Such a microarchitecture is a result of an evolutionary design for an ideal impact-resistant material providing armor to the mollusk (16, 17). Small inorganic particles could be synthesized by many species of bacteria and algae, and these particles could be oxides, sulfides, carbonates, or phosphates (1, 2). These particles have highly intricate architectures and are ordered during assembly. In many cases, the particles have a well defined shape formed within a certain size range and have orientational (when they are crystalline) and geometrical (even when noncrystalline) symmetry. These structural features are species-specific, and all are thought to originate in the macromolecules that control particle synthesis. For example, in Aquaspirillum magnetotacticum, a magnetotactic bacterium, small magnetite particles form within cytoplasmic vesicular compartments (magnetosomes) in ordered geometries (3), and these particles are perfectly crystalline (Fig. 1C). The magnetic particles are magnetic-sensing devices that steer bacteria toward anaerobic sediments. Singlecrystalline semiconducting particles, e.g., CdS, are synthesized in algae as a result of a toxification mechanism (18). Actinopoda and diatoms, single-celled organisms, synthesize amorphous siliceous units that are resting spores with highly intricate and symmetrical geometrical shapes (Fig. 1D). Similar structural skeletal units, spicules of SrSO4, are found in Acantharia (19). The cyst around a chrysophyte is a protective shell-like wall made of amorphous silica with elaborate geometries (4). Finally, in some cyanobacterial species, an outer cell surface proteinaceous membrane, an S layer, is a template for calcium-sulfateycarbonate synthesis. The thin layer of inorganic shell is a protective covering, consisting of highly organized two-dimensional ordered tiles (tessellations; ref. 6). Based on their observations, Klaus et al. (7) note potential uses of bacteria for nanostructured thin film or particulate materials synthesis to support technological applications. These uses, in fact, are exciting prospects for all hard tissues in that the understanding of the principles of ultrafine particle (and hard tissue) synthesis could potentially be exploited in materials sciences. The use of biological principles in materials formation is an emerging field called biomimetics (9, 10). The