APPENDIX F Bioinspired and Bioderived Materials

In this detailed appendix the Panel on Bioinspired and Bioderived Materials examines what organisms can do, and it takes a flight of fancy to suggest what can be “borrowed” for advanced materials or processes. The panel writes from the perspective of what biology does, rather than what defense needs are, because it does not know what applications will arise from the use, adaptation, or mimicry of any given biological structure or design. Even where an application can be imagined with some specificity, it would be a mistake to assume it to be the only application that could arise from that biological model. Examples are

  • Atomic level control of structure—materials by design. One of the most striking capabilities of living organisms is their ability to produce extraordinarily complex molecules with virtually error-free control of the location of each constituent atom, down even to control over the synthesis of one or another optical isomer. Molecules display sophisticated functions because each of their thousands of atoms has been placed in a precise, predetermined position in the molecule. Further, organisms design molecules they need, with the properties required, by controlling the number, type, and arrangement of their atoms. Through enzyme catalysis and templated synthesis (see below), organisms make exactly what they need with little waste, a production scheme that is clearly a model for in vitro synthesis. This control of structure at the atomic level is also a way to address the critical issue in, for example, the ceramic or metal-processing goal known as net shape manufacturing, where



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APPENDIX F Bioinspired and Bioderived Materials In this detailed appendix the Panel on Bioinspired and Bioderived Materials examines what organisms can do, and it takes a flight of fancy to suggest what can be “borrowed” for advanced materials or processes. The panel writes from the perspective of what biology does, rather than what defense needs are, because it does not know what applications will arise from the use, adaptation, or mimicry of any given biological structure or design. Even where an application can be imagined with some specificity, it would be a mistake to assume it to be the only application that could arise from that biological model. Examples are Atomic level control of structure—materials by design. One of the most striking capabilities of living organisms is their ability to produce extraordinarily complex molecules with virtually error-free control of the location of each constituent atom, down even to control over the synthesis of one or another optical isomer. Molecules display sophisticated functions because each of their thousands of atoms has been placed in a precise, predetermined position in the molecule. Further, organisms design molecules they need, with the properties required, by controlling the number, type, and arrangement of their atoms. Through enzyme catalysis and templated synthesis (see below), organisms make exactly what they need with little waste, a production scheme that is clearly a model for in vitro synthesis. This control of structure at the atomic level is also a way to address the critical issue in, for example, the ceramic or metal-processing goal known as net shape manufacturing, where

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the product is produced in the shape required, rather than being machined after production. Adaptation to the environment. Organisms sense their environments (see below) and alter their properties to adapt to them. Shifting humans to high altitude, for instance, increases the production of the molecule 2,3-bisphosphoglycerate, which binds to the protein hemoglobin in the blood, altering its shape to decrease its affinity and thus allowing the hemoglobin to deliver more oxygen to the muscles and brain. Amplification of signals. Blood clotting, gene expression, and the activation of enzymes in the control of cellular energy production all involve the amplification, by many orders of magnitude, of signals initiated by a very small number of molecules, photons, electrons, or ions. Amplification is a multistep pathway, each step activating an enzyme that then activates a very large number of copies of the next enzyme in the pathway. Amplification is often performed without additional energy input, a feature that has great potential value. Benign processing. Biological processes are generally less hazardous than their synthetic counterparts. Synthetic nanocrystals, which are of such great interest now, are synthesized at very high temperatures with hazardous precursors (see the work of Alivisatos at University of California at Berkeley, Bawendi at Massachusetts Institute of Technology, and Mirkin at Northwestern University). Organisms produce magnetic and semiconductor nanoparticles and other materials, often with great homogeneity, at room temperature and pressure (e.g., aquaspirillum magnetotacticum). Biocompatibility—interfaces with living and nonliving materials. Organisms have learned to control a wide variety of interfaces with disparate materials. Biomineralized tissues of a variety of compositions are in contact with organic materials in bone, teeth, and shell. On the other hand, the use of inorganic materials for implants, while successful in the short term, often encounters long-term problems at the interface with the living tissue. A great deal of effort is being expended to understand and mimic the structure and properties of mineralized tissues. The ability to “grow” armor (see Chapter 7) in specific shapes, much as a lobster does, would be of great benefit, as would the controlled growth of mineralized phases for functional thin films or particulate applications (Klaus et al., 1999). Phage display and other such techniques are being explored with some success (Seeman and Belcher, 2002) in the specific binding of proteins to semicon

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ductor and other nanocrystals. The crystalline ordering of the viral particles could allow the alignment of the nanocrystals in arrays that might have applications. Both of these efforts involve the ability to control the phases and precipitation of inorganic materials through the use of designed proteins. Attempts to make hybrid structures and devices composed of both inorganic and organic or cellular materials have also encountered difficulties, primarily in terms of long-term cell viability in such a foreign environment. This interface is becoming increasingly important because we must envision hybrid devices that exploit the many cellular functions that cannot yet be reproduced without the living cell but that are required for a particular function. For many years, whole cells have been attached to surfaces in bioreactors for fermentations. Hybrid circuits with both semiconductor chips and synaptically connected neurons have been explored. Nerve cells from the snail Lymnaea stagnalis have been immobilized, through nonspecific linkages, on silicon chips, using polyimides. Interfaces with the neurons were such that voltage pulses on the chip could excite the cells (Zeck and Fromherz, 2001). “Metabolic engineering” has been used to alter the surfaces of cells to improve their binding to specific sites on nonliving surfaces—metals, polymers, or ceramics—while the cells maintain their natural functions (see the work of Carolyn Bertozzi at University of California at Berkeley). Biodegradable materials. Living things, almost by definition, make biodegradable materials. Biosynthesis is accomplished almost exclusively by enzyme catalysis of chemical reactions. These types of bonds are also broken enzymatically, by enzymes widely present in the environment. A fundamental law of enzyme catalysis requires that enzymes increase the rate of the reaction in the forward (synthetic) direction to exactly the same extent as they increase the rate of the back (degradative) reaction. Biopolymers: control of properties. Biopolymer molecular back-bones are constructed of a far greater variety of monomeric units than are synthetic polymers and thus can have a far greater range of properties and can have those properties tuned to a much greater extent. Monomer placement in the molecular chain is, in most cases, precisely controlled, giving rise to macromolecules of exact chemical composition and degree of polymerization. Nucleic acids use five primary monomers and many others to a lesser extent. Proteins use 20 primary amino acids, some of which are modified after initial synthesis. Although some carbohydrates are

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composed of a single monomer, others draw from an alphabet of many more that vary in size, isomerization, charge, and functional group and each affect the properties of the polymer in a different way. Recent research has progressed well in expanding the number of monomeric units in both proteins and nucleic acids, allowing the incorporation of monomers with an almost unlimited variety of sizes or with specific redox, optical, electrical, magnetic, and chemical properties. Equally important to the materials properties of these polymers is the fact that biopolymers, whether nucleic acids, proteins, or carbohydrates, are made to a precise, uniform length, giving greater control of properties and also the potential for enhanced properties, alignment, and crystallization. Naturally occurring biopolymers do have a limited number of different backbone structures, but research has broadened this range, further increasing the breadth of properties that can be achieved. In addition, techniques are being developed to use these materials in unusual environments. Mirkin, for example, has developed a technology to “write” thin lines of proteins or nucleic acids on a variety of inorganic surfaces using the tip of an atomic force microscope as a quill and a solution of the polymer as the ink. —Nucleic acids. DNA and RNA are of course involved in the storage and use of cellular information, and RNA in catalysis and as scaffolds in supramolecular structures. These materials are found base-paired in the well-known “double helix” form of DNA or in single strands, which often, through the same mechanism, fold back on themselves. DNA double helixes are in fact structural materials, exhibiting the properties of long, relatively rigid rods with a persistence length of approximately 50 nm. Folded single strands, as in transfer RNA, form precisely determined three-dimensional structures. These structures are critical to the role of these molecules in genetic information storage and transfer, but they can also be exploited in other materials applications. Alivisatos, Mirkin, Seeman, Frechet, and others have linked nanocrystals or photoactive groups with electronic or optical properties to individual single strands of DNA of defined sequence and have synthesized structures through base pairing that link several single strands to align the active groups in precise positions in space. Some of these structures have demonstrated energy transfer from donor to acceptor groups, presenting intriguing possibilities for electronic structures. Ghadiri and others have developed systems that exploit the base pairing capability of DNA for rudimentary “computing” devices (Mao et al., 1999). These results are tantalizing at best, with no

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clear path to application, but no clear evidence exists that applications cannot be achieved. —Proteins. Driven by their amino acid sequence, proteins fold into precise three-dimensional shapes. The range of properties that these polymers exhibit or contribute to is enormous, including lubricity, adhesion, viscosity, stiffness, toughness, flexibility and other mechanical properties, clarity, and, in the case of aspartame, taste. Color. We have all come to admire the beauty of the colors of living organisms, but of greater interest is the potential to mimic their use of color as a functional property. Some organisms, for example, can alter the molecular structure of their surfaces to alter their appearance as protection from predators. Certain birds (e.g., peacocks), fish, snakes, and butterflies appear colorful not (only) because they have pigments but because their overlapping carbohydrate scales impart iridescence by creating interference patterns that give the appearance of different colors depending on the angle of viewing, the wavelength of the light illuminating them, and the medium they are immersed in. The color observed can also be altered by changing the refractive index of the liquid between the layers. Use of a solvent with the refractive index of cuticle results in the complete loss of constructive interference, no iridescence, and only the dull brown color of melanin. Chameleons change in response to changes in light and temperature (not, apparently, to blend in with their surroundings) through their control of the extent to which various layers of colored or reflecting cells below their skin are exposed to the surface. Work on this control of color, which has obvious defense applications for uniforms and equipment paints, is progressing in a number of laboratories, including those of Gregory at Clemson, Hanks at Furman, and Samuels at Georgia Institute of Technology in a search for polymers that change their response to electromagnetic radiation in the presence of applied electrical or magnetic fields. Catalysis/enzymes. Biocatalysis is an exceptionally efficient manufacturing process. Biocatalysts accelerate reactions by up to 13 orders of magnitude, with exquisite specificity for starting materials and products (producing no byproducts), at room temperature and atmospheric pressure. The activity of enzymes can be controlled over several orders of magnitude through the binding of specific effector molecules. Selective activation of enzymes could effect specific chemical conversions of munitions, therapeutic agents, and odorants. Harnessing these materials would be nothing short of revolutionary.

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Combinatorial synthesis. Each of us carries in our blood stream more than a hundred million different antibody molecules, all with slightly different structures. As a result, in virtually all cases, there is an antibody that can bind, jigsaw-puzzle-like, to an invading virus or bacterium and inactivate it. This parallel synthesis of a huge variety of extremely similar structures can have great impact on development of materials. In many cases, the current state of theory and modeling is too primitive to allow prediction of the structure of a single optimal material with the desired mix of properties. Battery manufacturers have recently announced that their next-generation cells will contain materials discovered through combinatorial methods. Computation. The holy grail of computer designers remains a device that mimics the human brain. Nothing comes close to the brain’s ability to store and retrieve information, often from apparently unrelated “data entry” events. Its ability to focus on a subset of the huge number of stimuli and inputs it receives at any one time is also unmatched, as is its ability to “reason” by combining bits of information and weighting them appropriately as it sums their input into the solution of a problem. No device competes in use of spoken language. It is true that silicon computers are already orders of magnitude faster than the brain; the brain’s capabilities rely, in part, on its ability to process in parallel. A number of biological materials are being studied for brain-like properties. The protein bacteriorhodopsin has been shown to have the capability for holographic data storage. There are initial reports of “DNA computers.” Clearly, an understanding of how the brain does parallel processing and the mechanism of the self-assembly of the billions of neurons into a functioning brain will be of great benefit, with many as yet undefinable applications. Conformational change. Many of the responses to external stimuli that have been discussed in other sections of this text (adaptation, sensors, smart materials) are based on the fact that proteins can alter their structure, and therefore their properties, in response to external stimuli. The response is mediated through the binding of one or more molecules from the environment at a specific site on the protein. Enzyme activity is regulated in this fashion, with the protein shifting from an active conformation to one that is less effective in binding the substrate, performing the chemistry of the reaction, or both. The oxygen-binding protein hemoglobin also exhibits the effect. On a shorter time scale than that for the increase in the concentration of 2,3-bisphosphoglycerate, hemoglobin binds to single protons. In

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low-proton environments like the lungs, it assumes a conformation that enhances its ability to bind oxygen. In the more acid environment of the muscles, however, there is a higher concentration of protons. These bind hemoglobin and cause it to change shape, making it less able to bind oxygen. The oxygen it had bound in the lungs is released so it can be used in the metabolic processes that create the energy required for muscle contraction. Energy conversion. Chemical energy powers organisms without the use of flammable fuels and the volatility and heat of reaction associated with those fuels. Molecular motors, described elsewhere, convert chemical energy (in the form of ATP) directly into mechanical energy, bypassing the heat production step of conventional motors and engines. The photosynthetic sequence of light energy capture, production of “high energy” chemical stores, and the oxidation of those stores to produce metabolic and mechanical energy is one that, if harnessed, would revolutionize energy conversion. Much work is progressing on photosynthetic mimics, both biological and inorganic photovoltaics. Though many are remarkably efficient mimics of aspects of the process, much remains to be done. Evolution. All too often we encounter materials that are ideally suited to perform in the environments for which they were originally designed but poorly suited to new environments that arise later. Species evolve constantly to allow them to survive in new environments. Each population includes individuals with minor variations from the norm in virtually every property. A change in environment increases the relative reproductive success of one such variant, which then moves to dominate the population. Evolution has been recreated in controlled environments for experimental purposes. It has also been employed in the “maturation” and optimization of antibodies and other proteins, where the continual production of variants and the selection of the “better” variants has led to better products. Defense systems capable of evolving would be of obvious value. Extreme environments. In general, biological systems are regarded as impractical for many applications because of their sensitivity to extremes of environment. On the other hand, organisms have adapted to live in the below-freezing waters of Antarctica or the ocean depths and in the near-boiling conditions of hot springs or deep-ocean thermal vents. Those living at the ocean depths are protected against exceptionally high pressures, those living in salt flats are protected from high osmotic pressure, those that line the stomach are adapted to extreme acidity, and others are

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exceptionally resistant to ionizing radiation. In each case, specific protective mechanisms have evolved. In principle, transferring these to organisms or systems with the required properties could protect them from these extreme environments. Hierarchical construction. Biological structures are extraordinarily complex, far more so than synthetic systems, and their sophisticated properties reflect that complexity. However, their synthesis is usually far less complex, relying on sequential hierarchical construction principles. For example, the synthesis of collagen fibers, whose thickness can be measured in millimeters, can be simply described as a sequence of construction steps, starting with the association of individual atoms and then associating the resulting structures in an increasing complex manner. The path is programmed into the structure of the material, allowing great complexity of result with minimal complexity of design. Lightweight materials. Living systems are inherently lightweight. They use almost exclusively the first row elements—carbon, hydrogen, nitrogen, oxygen—with lesser amounts of phosphorus and sulfur and very small amounts of others. Our ability to mimic living systems and create structural and functional materials from these elements would lead to enormous reductions in fuel use, and in the weight carried by the highly equipped modern soldier. Lubricants. Enormous inefficiencies, loss of function, and expense result from inadequate lubrication of the contact surfaces of moving parts. Living systems, which must solve the same problems, have evolved molecules to lubricate joints, portions of the eye, and internal organ surfaces. These usually highly charged molecules could be models for biomimetic lubrication. Hyaluronic acid, for example, which is strongly anionic is an important component of the synovial fluid that lubricates the joints. Mass production. Large-scale production of materials can often be expensive. Regulatory mechanisms in organisms allow for the production of defined levels of each molecule made, using “inducers” or “repressors” and “weak promoters” and “strong promotors.” Levels of product production approaching tenths of total cell volume can be achieved. Several years ago, the genes for the natural plastic polyhydroxybutyrate were transferred into plants. Acres of farmland devoted to these transgenic plants could be inexpensively harvested and the polymer extracted. Genes for proteins are now being inserted into goats or cows in a way that leads to their secretion

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into the easily collected milk, which, of course, can be “grown” for the cost of animal feed. Membranes. The cell membrane is an extraordiary multifunctional structure. It defines the selectively impermeable boundaries of cells. It helps define the surface topology of cells; houses transport systems to move materials in or out; and incorporates motors, rotors, energy-producing devices, and exquisitely sensitive, selective sensors. It creates nonpolar compartments in the midst of a fully aqueous environment. It is self-healing and self-assembling, can grow as the cell it surrounds grows, and can split into two as the cell divides. Membranes are highly flexible and can adapt their shape to a variety of structures and also to perturbations in those structures as the cells progress through the various stages of their lives or perform their myriad functions. They are also quite robust, despite the fact that the individual component molecules are not covalently linked to each other. A great deal of effort has gone into the mimicking of the cell membrane, much of it successful. Artificial self-assembled monolayers are used in a wide variety of efforts to study self-assembly or other membrane-associated properties. Membrane mimics are made with artificial molecules, mirroring the self-assembling amphiphilic properties of membrane lipids but incorporating greater rigidity through cross-linking, or functionality through light-absorbing chromophores, inserted channels, or molecular recognition groups. Use of other molecular components allows for multilayered membranes with their own sets of properties. Molecular recognition. Individual biological molecules have the extraordinary ability to recognize specific other molecules in a sea of very similar structures. This is the basis for the functioning of the cell membrane as a biosensor, the structure and replication of DNA as a genetic or structural material (see nucleic acids), and the specific catalysis of enzymes. The mechanism of this recognition involves several factors. The first is a geometric fit similar to that between two pieces of a jigsaw puzzle. Then, along the surface between the two bound molecules are complementary binding groups: Positive charges on the face of one molecule are adjacent to negative charges on the other molecule. Other forces to enhance binding, including hydrophobic interactions and polar interactions, are also found along the interface. Complexity is added by the fact that proteins are not fixed in shape but are quite flexible; they rapidly and spontaneously interconvert among a set of possible conformations. Gener

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ally, only one conformation of a given protein binds a particular target molecule, and the binding of that molecule locks the protein into that particular configuration. This is a powerful tool in protein design and function but it does add complexity to the task of designing proteins for specific molecular recognition functions. Motors, rotors, pumps, transporters, tractors, springs, ratchets, contractile proteins. Cellular function depends on a variety of motors, rotors, and related devices that use chemical energy to move ions, macromolecules, organelles, chromosomes, and even whole cells. A newly characterized motor packs DNA into the heads of viruses using 60 pN of force (Smith et al., 2001; Cluzel et al., 2000; Stock et al., 1999; Keller and Bustamante, 2000). The enzyme ATP synthase and the various components of the electron transport chain are themselves molecular pumps and motors, embedded in the inner membrane of the mitochondrion and using metabolic energy to pump protons across the membrane. Protons flow spontaneously back across the membrane, but only through the synthase, which rotates in response to that flow of protons. This rotation has been shown by Oster (Elston et al., 1998) and others to drive the synthesis of ATP. In reverse, using ATP releases energy for the rotation of the protein and the pumping of protons out across the membrane. Another rotational motor embedded in the cell membrane drives the high-speed rotation of flagella, the tails of bacterial cells that enable them to “swim” toward nutrients and away from repellants. Linear motors like myosin and kinesin move subcellular structures by direct conversion of chemical energy to mechanical energy. To a great extent, the nature and structure of the molecules involved in these functions are understood and some manipulation has been achieved. Techniques like single-molecule spectroscopy allow the study of individual motors and rotors. Other techniques allow investigators to anchor these structures to solid supports and to pull on them and treat them in effect like springs, relating the force applied to the extension of the molecule. Mahadevan and Matsudaira (2000) have shown that small changes in protein subunits amplified by linear arrangements in the filaments can lead to structures that store energy and then release it on demand, creating movement. The interfacing of millions of these efficient biological devices to produce “macro” levels of power is not impossible by 2020. Multifunctional materials. Another holy grail of materials research is materials that perform several functions simultaneously. Here biological systems again point the way. Skeletal plates on the arms of the brittle star

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provide not only structure and protection but also focus light on nerve receptors beneath, somewhat like a compound eye (Sambles, 2001). Multifunctional scales coat the wings of butterflies, supporting the aerodymnamics of the wing while assisting in temperature control of the butterfly and providing wing colors and patterns that act as a defense mechanism against predators. Nanoscale synthesis and function. The revolution in nanoscience allowing the synthesis, characterization, and use of structures of dimensions 1-100 nanometers is having a major impact on a wide variety of fields. At these dimensions, the properties of an ensemble of molecules are controlled by surface rather than bulk properties, allowing properties of a single molecular composition to be tailored over a broad range. “Small” molecules like amino acids, lipids, and sugars are of single nanometer dimensions and proteins can range from 10 to 100 nanometers in diameter, making them ideal components of these systems. Self-assembly. Perhaps the most interesting property of biological systems is their ability to assemble individual molecules into large, complex, functional structures. Membranes assemble themselves because the lowest energy state of their component nonpolar molecules is the membrane structure itself. The assembly of biological molecules is directed by site-specific chemistry, while the assembly of synthetic polymers is often determined by external forces and statistical physics. Proteins composed of multiple individual proteins self-assemble, aligning the individual subunits precisely with respect to one another to perform a function as dependent on the relationship of the individual molecules as a watch is dependent on the positioning of its gears. Self-healing, repair, damage/fault resistance/tolerance. Living organisms are capable, to varying degrees, of self-repair and healing. Simple or very young organisms can replace entire sections of their bodies; more complex or older organisms are more limited, although the human liver, for example, can regenerate itself even after much of it has been removed because of damage or the need for donation as a transplant. On a more molecular level, membranes can repair holes and proteins can refold after being denatured. DNA polymerase, which copies DNA, reviews its own work, tearing out errors and replacing them with the correct base. Smart materials/sensors. Smart materials are those that alter their structure and properties in an almost immediate response to a change in their environment. In many cases these changes are reversible, in some cases, to varying degrees depending on the extent of the change in the

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environment. In some cases the response is triggered by physical changes, such as optical, electrical or mechanical effects. In other cases, changes in the levels of specific chemical substances are detected. These “analytes”are detected by proteins and carbohydrates (receptors) whose structure is defined at the level of each atom and the spatial relationship between atoms. They are embedded in the cell membrane and extend beyond its outer surface to bind the target with high affinity and specificity (see molecular recognition, above). In some cases the response to the change is functional. In other cases, it is simply a record of the change. In bacteria the enzyme glutamine synthetase monitors the level of nine independent factors in its environment and adjusts its rate of catalysis on the basis of a summation of these inputs. Entire metabolic pathways respond to single molecules, such as hormones or growth factors. Most of these responses are triggered by alterations in the shape of the receptor on binding its target. The ability to change chemical activity, color, electrical conduction, and mechanical properties in response to changes in the environment would be valuable in a variety of applications. Perhaps the most advanced smart materials at this time, however, are sensors, which translate their detection of defined targets into measurable optical, electrical, or mechanical changes. In many cases, other organisms demonstrate discrimination and sensitivity sometimes approaching the detection of single molecules or photons. In principle, individual soldiers could distinguish friend or foe from a distance when sight and hearing are limited. Chemical or biological agents could be detected before their concentrations reach toxic levels. A wide variety of mechanisms have evolved to achieve this detection, and any one could be an important application. As miniaturization progresses and micro- and nanoscale devices are devel-oped, sensors for extremely small forces will be required. Recent work has shown that the unfolding of single strands of RNA, which involves only the breaking of a number of hydrogen bonds, can be measured using optical tweezers, allowing us to speculate that these measurement tools could be adapted as mechanical sensors. In other work, cantilevers have been shown to allow the detection of the change in energy resulting from the binding of very small numbers of molecules, again allowing speculation about new, ultrasensitive mechanical sensors. The Melanophila beetle senses IR emission of a forest fire from 50 km. Vipers, pythons, and other snakes strike objects on the basis of their detecting minute differences radiated in temperature, with discrimination levels in the thousandths of a

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degree centigrade. Although investigators have had difficulty adapting this and similar systems to working devices, these problems may well be resolved by 2020. Structural materials. As described in other sections of this report, spider dragline silk, synthesized primarily from carbon, hydrogen, oxygen, and nitrogen, has long been envied for its strength-to-weight ratio, which exceeds that of steel. Other structural fibers, such as collagen and keratin, could find applications if their synthesis were within reach. Research is progressing in the use of synthetic materials to mimic biological models, for example, hydrogels that can reversibly bind water to mimic the ability of collagen to absorb shock. Extensive work has been proceeding for decades to improve our understanding and ability to mimic the “hard” materials like bone, teeth, and shell, which have exceptional combinations of mechanical properties and light weight, but they still elude our grasp. Mineralized components are usually made, as are the organic components, of a small group of simple compounds like hydroxy apatite, calcium carbonate, or phosphate. They do, however, form a wide variety of structures, with a wide variety of properties, performing a wide variety of functions, because the organic phase of protein controls the crystal structure of the mineral and a variety of such structures are possible. Hydroxy apatite, for example, is the mineral in both teeth and bone, materials that have vastly different mechanical properties. Progress is being made in our understanding of these materials. For example, Morse (2001) has recently shown that the synthesis of the silica needles in a marine sponge is achieved by the catalytic polycondensation of silicon alkoxides. The catalysts are aligned in linear repeated assemblies of the enzyme in the form of a rod, allowing the deposition of the rodlike spines around them. Morse reveals new routes to the synthesis and structural control of silica and polysilsesquioxanes. Systems. On a larger scale, the performance of biological systems often exceeds that of current technology. Sharkskin, for example, exhibits better hydrodynamic behavior than polished surfaces, an effect attributed to the organization and structure of the surface. Lotus leaves are remarkable in their ability to reject dirt. Their fine surface roughness prevents tight binding of dirt particles (and even glues), which are washed away by water repelled by the waxy coating (Barthlott and Neinhuis, 1997). Structural surfaces on insect legs allow for reversible adhesion, as do the microscopic setae on the feet of geckos, which can hang upside down and walk over almost any vertical wall (Autumn et al., 2002).

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Templated synthesis. Much of biological synthesis occurs through enzyme-catalyzed reactions, with the great specificity of these catalysts providing high efficiency and minimization of byproducts. Equally high fidelity is achieved through templated synthesis, with the product produced through its specific match to a preexisting model. This is true of DNA and RNA synthesis, with a single strand determining the sequence of bases to be organized in the daughter strand. It also occurs in the production of of mineral phases that are directed by underlying proteins (Mann, 1988; Knight et al., 1991; Addadi and Weiner, 1985; Sarikaya, 1999). This strategy could be valuable for the synthesis of numerous types of materials for defense applications. Transport systems. Living organisms must transport a wide array of molecules and structures, both in and out of the organism or its constituent cells and to specific locations within the organism or its cells. Membranes are extraordinarily selective in allowing materials to penetrate and pass through. Some even prevent the hydrogen ion from passing. On the other hand, membranes can create systems to specifically allow the passage of molecules of choice. In many cases these “channels” open or close in response to either voltage changes or the presence of other molecules. We might imagine clothing designed to allow moisture to pass through while blocking the transport of specific toxic agents. Finally, in some systems the channels are energized, allowing the buildup of concentration gradients. REFERENCES Addadi, L., and S. Weiner. 1985. Interactions between acidic proteins and crystals—Stereochemical requirements in biomineralization. Proc. Natl. Acad. Sci. 82(12):4110-4114. Barthlott, W., and C. Neinhuis. 1997. Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202(1):1-8. Cluzel, P., M. Surette, and S. Leibler. 2000. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287(5458):1652-1655. Elston, T., H. Wang, and G. Oster. 1998. Energy transduction in ATP synthase. Nature 391(6666):510-513. Keller, D., and C. Bustamante. 2000. The mechanochemistry of molecular motors. Biophysical Journal 78(2):541-556. Klaus, T., R. Joerger, E. Olsson, and C.G. Granqvist. 1999. Silver-based crystalline nanoparticles, microbially fabricated. Proc. Natl. Acad. Sci. 96(24):13611-13614. Knight, C.A., C.C. Cheng, and A.L. Devries. 1991. Adsorption of alpha-helical antifreeze peptides on specific ice crystal-surface planes. Biophys. J. 59(2):409-418. Mahadevan, L., and P. Matsudaira. 2000. Motility powered by supramolecular springs and ratchets. Science 288(5463):95-99.

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Mann, S. 1988. Molecular recognition in biomineralization. Nature 332(6160):119-124. Mao, C.D., W. Sun, Z. Shen, and N.C. Seeman. 1999. A nanomechanical device based on the B-Z transition of DNA. Nature 397(6715):144-146. Morse, D.E. 2001. Biotechnology reveals new routes to synthesis and structural control of silica and polysilsesquioxanes. The Chemistry of Organic Silicon Compounds, Z. Rappoport and Y. Apeloig, eds. New York: John Wiley & Sons. Sambles, R. 2001. Optics: Armed for light sensing. Nature 412(6849):783. Sarikaya, M. 1999. Biomimetics: Materials fabrication through biology. Proc. Natl. Acad. Sci. 96(25):14183-14185. Seeman, N.C., and A.M. Belcher. 2002. Emulating biology: Building nanostructures from the bottom up. Proc. Natl. Acad. Sci. 99:6451-6455. Smith, D.E., S.J. Tans, S.B. Smith, S. Grimes, D.L. Anderson, and C. Bustamante. 2001. The bacteriophage phi 29 portal motor can package DNA against a large internal force. Nature 413(6857):748-752. Stock, D., A.G.W. Leslie, and J.E. Walker. 1999. Molecular architecture of the rotary motor in ATP synthase. Science 286(5445):1700-1705. Zeck, G., and P. Fromherz. 2001. Noninvasive neurielectronic interfacing with synaptically connected snail neurons immobilized on a semiconductor chip. Proc. Natl. Acad. Sci. 98(18):10457-10462.

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