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• W3014331118 abstract "At this point, the terms “bio-inspired” or “biomimicry” are near cliché. People have been turning to nature for inspiration to help them solve problems for millennia. Humankind is nature’s ultimate scribe. From buildings and bridges, materials and medicine, and architecture and art, designers, scientists, and engineers continue to study the complex solutions nature has devised to persist, develop, and evolve. The pursuit of life and physical sciences stem from an innate desire to understand how the world works, so it is no surprise that nature is a continuous source of both motivation and mystery. Beyond the artistic, the underlying rules of biology—the chemistry, physics, mechanics—have been difficult tomes to decipher. Recently, learning from nature has been used as a powerful approach to develop emerging materials and structures with new properties and excellent performances. At this point, the terms “bio-inspired” or “biomimicry” are near cliché. People have been turning to nature for inspiration to help them solve problems for millennia. Humankind is nature’s ultimate scribe. From buildings and bridges, materials and medicine, and architecture and art, designers, scientists, and engineers continue to study the complex solutions nature has devised to persist, develop, and evolve. The pursuit of life and physical sciences stem from an innate desire to understand how the world works, so it is no surprise that nature is a continuous source of both motivation and mystery. Beyond the artistic, the underlying rules of biology—the chemistry, physics, mechanics—have been difficult tomes to decipher. Recently, learning from nature has been used as a powerful approach to develop emerging materials and structures with new properties and excellent performances. My formal undergraduate training was in structural engineering—bridges and buildings, concrete and steel—so it took a few odd grad school turns to get to nature. If you really want to make an efficient structural design, you need to intimately know how your materials will deform and (ultimately) fail. Thus, my specialty and expertise deviated from structural design to mechanics of materials. From there, the world of materials science provided a vast library of materials behaviors to explore, and there are far more interesting materials than steel alloys and cementitious systems. Although exotic metals and plastics/polymer materials provide their own set of challenges, the superlative properties of biological materials were low-hanging fruit, ripe to be investigated. While I was a doctoral candidate and carrying into my work as a PI, I did a little bit of work on the mechanics and failure of spider silks and webs.1Cranford S.W. Tarakanova A. Pugno N.M. Buehler M.J. Nonlinear material behaviour of spider silk yields robust webs.Nature. 2012; 482: 72-76Crossref PubMed Scopus (334) Google Scholar The topic spurred the imagination of many students, because spiders and silks were both so tangible yet had an unknown, almost Lovecraftian-like quality. The most frequent question I was asked was why, as a structural engineer, was I studying spider silks? My answer was always “we don’t study silk to swing from a building like Spiderman, we study silk to learn from nature.” The point being, of course, that the biological purpose of spider silk—in web building and prey capture—is not what makes it interesting to materials scientists, it is how those goals are achieved. Man-made structures look nothing like nature. Where nature has curves, man has right angles. Everything aligned and orthogonal. Usually, we use a single material (steel, for example), and our functional systems are separate (HVAC, electrical, water, etc.). Although our structures are strong and durable, it comes at a price of permanence, lacking the ability to adapt or heal. Indeed, at first glance, nature does not have much to offer a steel or concrete building. What can gluey, sticky, thread-like spider silks offer? From the right perspective to structural engineering, everything can be a beam. While multifunctional, even those silk threads act as beams—load-carrying members providing structural integrity for a web. One of our pioneering studies on the failure of spider webs indicated that the characteristic hyperelastic constitutive response of silk-facilitated localized failure. The material behavior of the silk “beams” resulted in a concentrated “damage zone.” If the “beams” were steel, this would not have occurred. Taking this concept, one could easily introduce damage-localizing energy dissipation mechanisms into traditional structural designs (such as well-known shear fuses). The function—local failure—is removed from the material (silk or steel alike). At the same time, we are stealing a lesson from nature, by learning how biology seamlessly integrates materials and function. Most synthetic materials are not intrinsically functional. Rather, we seek out desirable properties and then determine (or design) a functional role for that material. Consider copper, for example. Lying in the ground as a metal, there is no function of copper. For hundreds of years, it was known as a relatively workable metal, leading to early copper tools. Once we discovered electricity and measured the conductivity of copper, the predominant application changed from bronze to electrical wiring and circuit boards. We found a function to fit the properties. Compare that to a biological material such as bone. Bone is primarily a structural member for living beings—a scaffold to affix tissue and other organs. It does not exist beyond this role—it was evolved and grows specifically to serve this function. The link between material and function exists for all biological materials, including teeth, hair, skin, blood vessels, etc. Nature does not mine them and assign function due to their properties, their properties evolve towards their ultimate function. This is a truly mind-bending paradigm! To appreciate the material structural-functional links, a holistic perspective is necessary. One cannot consider the material independently from its physiological role. They are intimately linked in a complex and reciprocal manner. This perspective has been termed “materiomics”—the holistic study of material systems; the examination of links between physiochemical material properties and material characteristics and function; and the focus on system functionality and behavior, rather than a piecewise collection of properties, a paradigm similar to systems biology.2Cranford S.W. de Boer J. van Blitterswijk C. Buehler M.J. Materiomics: an -omics approach to biomaterials research.Adv. Mater. 2013; 25: 802-824Crossref PubMed Scopus (99) Google Scholar Moving away from total mimicry, materiomics attempts to move toward understanding the rules that underwrite nature’s processes. Once we start to look across multiple biological systems—start looking at materials systems—we start to see repeated patterns and fundamental “design” rules that have evolved to fulfill multiple biological roles. By no means definitive, four common material rules that are encountered in many biological systems with potential to be exploited in synthetic systems are as such: (1) multifunctional, (2) architected, (3) disordered, and (4) energetic, i.e., Nature MADE (Figure 1). Back to the beam analogy, if you look at the typical construction of a high-rise (sometimes exposed in the basements or parking garages) you can clearly see the structural elements (e.g., beams, columns, joists, girders, shear walls, braces, etc.) decoupled from the functional systems (e.g., water supply, wastewater, electrical, communication, etc.). The structural people do not have a need to talk to the HVAC people—the jobs (and thus designs and contract bids) are independent. Clearly, in this multitasking world, this is inefficient. Nature has figured this out long ago. Although bone was mentioned a little earlier, many other structural biological materials (e.g., shells, scales) are often multifunctional, simultaneously offering mechanical protection and performing other functional roles such as hydrodynamic drag reduction,3Domel A.G. Saadat M. Weaver J.C. Haj-Hariri H. Bertoldi K. Lauder G.V. Shark skin-inspired designs that improve aerodynamic performance.J. R. Soc. Interface. 2018; 15: 20170828Crossref PubMed Scopus (72) Google Scholar coloration, or even optical sensing.4Aizenberg J. Tkachenko A. Weiner S. Addadi L. Hendler G. Calcitic microlenses as part of the photoreceptor system in brittlestars.Nature. 2001; 412: 819-822Crossref PubMed Scopus (509) Google Scholar A recent paper in Matter has demonstrated that even teeth can be multifunctional—not only for killing prey and masticating food, but also acting as camouflage. The teeth of the deep-sea dragonfish have evolved to be not only tough (with a human-like dentin structure) but also transparent, hiding the fish in the darkness of the ocean depths from prospective meals. Although this might seem only useful for a deep-sea fish, it paves the way for biomimetic tough, transparent ceramic materials.5Yin Z. Hannard F. Barthelat F. Impact-resistant nacre-like transparent materials.Science. 2019; 364: 1260-1263Crossref PubMed Scopus (186) Google Scholar If you have to wonder where such a tough-yet-transparent material would be useful, take a quick look at your smartphone screen! One of the clichés of biological materials publications is the “hierarchical multiscale figure” that starts with a molecular structure, illustrates different assembled structures across scales, and ends with a cute representative photo of the organism. See, for example, studies on spider silk, nacre, crustacean shells, fish scales, insect cuticles, hair, wood, mussel byssus, sea sponges, muscle tendons, gecko setae, bone, and teeth, to name a few. There a few hypotheses for these multiscale hierarchies. First, they are a byproduct of the bottom-up assembly processes of nature, otherwise known as growth. Different structures are formed by a range of driving processes and mechanisms, resulting in a necessary component-based assemblage. Second, the hierarchies enable subtle variation at different scales, resulting in completely different emergent materials with the same fundamental components at the atomistic scale. One need only consider the range of protein-based materials to illustrate this fact—from elastin to microtubules to actin filaments—all ultimately constructed with the same set of amino acids. This is sometimes referred to as the universality-diversity paradigm, a materials framework based on the universality and diversity of its fundamental structural elements and functional mechanisms. Throughout nature, a limit set of elementary building blocks underlay extremely robust, multifunctional materials by self-organization of structures over many length and timescales, from nano to macro. Some of the structural features are commonly found in many different tissues and are highly conserved. Understanding, exploiting, and ultimately designing these building blocks (and their possible architectures) is a widespread strategy for bio-inspired materials. Turning to synthetic materials, we see the same emerging design technique resulting in the emergence in architected materials and metamaterials, wherein structure, not only underlying chemical components, dictate properties and behaviors. Metamaterial surfaces, for example, manipulate incident light waves via topology and can be used to influence radar design, subwavelength imaging, and even invisibility cloak design.6Krasnok A. Tymchenko M. Alù A. Nonlinear metasurfaces: a paradigm shift in nonlinear optics.Mater. Today. 2018; 21: 8-21Crossref Scopus (314) Google Scholar Only advances in synthesis and assembly procedures have made such structures possible. At the nanoscale, one of the most prevalent architected material types are MOFs, i.e., metal-organic frameworks.7Cai Z.-X. Wang Z.-L. Kim J. Yamauchi Y. Hollow Functional Materials Derived from Metal-Organic Frameworks: Synthetic Strategies, Conversion Mechanisms, and Electrochemical Applications.Adv. Mater. 2019; 31: e1804903Crossref Scopus (301) Google Scholar MOFs are a class of compounds consisting of metal ions or clusters coordinated to organic ligands to form one-, two-, or three-dimensional structures. Their highly porous yet chemical predictable structure leads to interesting applications in gas purification, gas separation, and catalysis as conducting solids and as supercapacitors. An assortment of different applications from common building blocks. Mother Nature would be proud. Nature, with complex hierarchical architectures and multifunctionalities, is also a relatively sloppy craftsman. Construction (i.e., growth) is typically rife with mistaken components, misalignments, and defects. Errors in the structure. This is one of the reasons why biological systems seem so organic in comparison to the orthogonal and precise geometries of engineered systems. Cells tend to aggregate seemingly haphazardly—the cellulose fibers across a tree section vary in diameter, similar to the osteons in a femur that vary in size.8Repp F. Kollmannsberger P. Roschger A. Kerschnitzki M. Berzlanovich A. Gruber G.M. Roschger P. Wagermaier W. Weinkamer R. Spatial heterogeneity in the canalicular density of the osteocyte network in human osteons.Bone Rep. 2017; 6: 101-108Crossref Scopus (43) Google Scholar Even with these non-precise arrangements, the structures still functionally work. The random arrangement of branched capillaries in the vascular system maximize not only the surface area necessary for exchange but also a level of redundancy and self-imposed pressure control. It provides a quite a challenging fluid dynamics problem. Precise arrangement requires an energetic cost—be it metabolistic, available resources, nutritional, or other thermodynamics limits. Simply put, an organism cannot smelt and heat treat bone like an alloy. To achieve consistent results, nature, rather than expend costs in construction, has evolved cleaver design rules to circumvent flaws. Nacre and bone, for example, have a characteristic soft-phase/hard-phase hierarchical structure, which is known to be mechanically flaw tolerant due to its intrinsic length scale.9Gao H. Ji B. Jäger I.L. Arzt E. Fratzl P. Materials become insensitive to flaws at nanoscale: lessons from nature.Proc. Natl. Acad. Sci. USA. 2003; 100: 5597-5600Crossref PubMed Scopus (1514) Google Scholar In synthesized materials, conditions are sometimes a little too perfect—constant dimensions with homogeneous compositions. This can result in relatively weaker behaviors, particularly with extremely small defects present. Consider the difference between a monocrystalline metal and another with a few added grain boundaries. A little disorder can turn a weakness into a strength. Materials live and die by their energetic requirements. Synthesis/growth? Energy requirement. Healing/re-bonding? Energy requirement. Ultimate failure? Energy requirement. Energy is the ultimate currency in nature, so it is not surprising it is highly regulated like the New York Stock Exchange. Focusing on one aspect, many biological materials have energy dissipation mechanisms that are “triggered” during failure. These include a combination of (1) weak bonding (e.g., H-bonds, disulfide bonds), (2) convoluted configurations (e.g., unfolding, helices, entropy), and (3) integration of multiple materials (e.g., the aforementioned soft-phase/hard-phase of nacre). Let us consider, as an example, the simple unfolding of proteins. Proteins are simply polypeptides, which are effectively long chains of amino acids. Depending on the sequence and the proclivity of the amino acids to attract, repel, bending, align, etc., the peptide chain folds into a particular structure (often with a particular function). Common motifs are so-called alpha helices, beta sheets, and omega loops. The primary bonding of these structures is hydrogen bonding (H-bonds), which are both (relatively) weak and reversible. One benefit is that the reversibility of the bonding enables repeated unfolding/folding cycles, which enables both large deformations and energy dissipation when subject to mechanical loads. A classic example of this unfolding mechanism is found in the protein titin—a giant protein, greater than 1 μm in length, that functions as a molecular spring—which is responsible for the passive elasticity of muscle in addition to keeping myosin molecules in place. Many studies have elucidated the characteristic sawtooth force-displacement unfolding of titin. Why is extreme elasticity advantageous? Simply put, extreme deformation facilitates graceful failure, rather than catastrophic rupture. Consider, as another example, an arterial aneurysm—i.e., a weakening of an artery wall that creates a bulge, or distention, of the artery. Although aneurysms are bad, the large deformation (facilitated by the energetic capacity of the tissue) is preferred over arterial fracture (and thus internal bleeding). The mechanical response provides a de facto “safety belt” for biological systems, enabling energy dissipation (via weak reversible bonding) over the one-and-done approach for engineered systems (where failure of strong bonds is irreversible). Such unfolding, deformation-based mechanisms are more frequently being employed in synthetic systems.10Deng Y. Cranford S.W. Tunable Toughness of Model Fibers With Bio-Inspired Progressive Uncoiling Via Sacrificial Bonds and Hidden Length.J. Appl. Mech. 2018; 85: 111001Crossref Scopus (4) Google Scholar Multifunctional. Architected. Disordered. Energetic. M… A… D… E… Nature MADE materials, just what we are looking for. Are these the only tricks nature has up its sleeve? Clearly not. These “design rules” are merely what I have seen over and over in the literature while I was still a researcher and what I have continued to see with submissions at Matter. Almost every paper that is submitted to Matter with a focus on biological materials can be loosely categorized into one of these ideas. We still have much to learn from biology, which has had an extensive head-start in research and development since the first single-celled organisms started replicating. Perhaps advances in machine-learning will uncover more design tricks, or computational methods will crack the complexity of living systems. We, as materials scientists and scientists alike, should not be satisfied with Nature “MADE” until we can adapt it to Nature “MAKE.”" @default.
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• W3014331118 title "Nature MADE: A Simple Guide to Biological Design Rules" @default.
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