Bioinspiration Across All Length Scales of Materials

Life appeared on earth more than 3.7 billion years ago.1 Since then, living organisms have constantly adapted to their environment, evolving into an incredible number of species. In this process, highly complex and multifunctional molecules and materials appeared and developed, fulfilling a wide variety of functions. They range from structural support, to sensing, locomotion, and more. In contrast, man-made materials can be optimized only for a limited degree of functionalities, and they are relatively simple when compared to the ones found in the living world. Nevertheless, increasing research efforts are directed toward functional or stimuli-responsive materials that can fulfil multiple or specific functions, adapt to their environment, or interact with biological systems, thus bringing synthetic materials a step closer to biological ones. Not surprisingly, materials scientists, chemists, physicists, biologists, and engineers nowadays look more often at the biological world to study and extract working principles in order to learn methods and concepts for the design and fabrication of novel materials. Some of these concepts are already a commercial reality: Velcro-based adhesives that imitate burrs interlocking into fur, or lotus-like superhydrophobic and self-cleaning surfaces found in glass coatings or façade paints, as well as car pigments mimicking the metallic blue appearance of the Morpho butterfly's wings. Nature is an inexhaustible source of inspiration for materials science well beyond these classic examples. Living organisms have evolved functional materials across all length scales: ranging from functional molecules and molecular machines (e.g., proteins), to self-assembled structures on the nano- and on the microscale (photonic structures, membranes, and reaction compartments such as organelles and cells, adhesive micro- and nanostructures, etc.) to the macroscopic length scale, which is often adopted by engineers, e.g., for load-bearing structures inspired by trees or the capabilities of plants to exert movement without hinges. This Special Issue of Advanced Materials presents bioinspired materials across all length scales, from the molecular level to large civil-engineering structures. Our collection of articles also demonstrates that a successful development and implementation of novel bioinspired functional materials requires a multidisciplinary approach that bridges the length scales and requires the collaboration of biologists studying the biological concept generators, chemists synthesizing novel molecules, physicists shedding light on structure formation on the nano- to microscale, and engineers implementing such novel materials into real-world structures. Bioinspiration can come in many forms, and it is often difficult to clearly define the term, especially as there are also other terms like “biomimetic materials” or “bionic materials” that describe similar ideas, sometimes even the same concept, in the scientific literature. Nevertheless, definitions and technical standards have been recently formulated.2-5 The basic rule to solve material challenges and to develop novel functional materials in a biomimetic way is to analyze a biological system, to abstract the underlying working principle into a model, and to apply this model to the design of a material, independently of their scale. However, in the literature, the term “bioinspired material” is often used in a much looser context to highlight analogies between the working principles of natural materials and synthetic materials, even if the latter were developed without following a biological role model. Nevertheless, such “inverse bioinspiration”, in which the biological system is only sought once the material has been developed, might be a valuable approach to understand the biological systems or to further refine the synthetic material. Before developing novel bioinspired materials it is highly recommended to consult biology for existing knowledge on biological concept generators. Wilts, Mayer, and co-workers (article number 1705322) demonstrate that even by focusing on the insect world, it is possible to identify a wide variety of functional materials and properties ranging from the thermal regulation strategies of ants, bugs, and bees, to the collective sensing behavior in many flying insects, to the hierarchical nanostructures that are responsible for the colors of butterflies and beetles. Beetles also retain the record of the whitest materials ever obtained with polymers. Wilts, Sepe, and co-workers unveil via cryo-ptychographic X-ray tomography the complex random network in the scales of Cyphochilus beetles responsible for their bright white appearance (article number 1702057). More sophisticated color-changing bioinspired optical materials are reviewed by Isapur and Lattuada, who provide an overview of recent developments of stimuli-responsive color-changing systems inspired by insect and animals (article number 1707069). Proteins are some of the most versatile and multifunctional-material-forming molecules in nature. For example, the underwater adhesion of mussels and sandcastle worms to the surface of rocks and sand grains is achieved by catechol-rich proteins that contain amphiphilic and ionic functional groups. Kamperman and co-workers review these natural adhesives, as well as synthetic polymeric systems that mimic their supramolecular operating principle (article number 1704640). A prime example for structural proteins is silk. Silk proteins are not only extracted from natural sources to create textiles, but also have remarkable properties as biomaterials because they are biocompatible and hypoallergenic. This makes them suitable for wound dressings, surgical sutures, or tissue-engineering scaffolds. Recombinantly produced silk proteins solve the problems associated with silk from natural sources, such as batch-to-batch variations and contamination with other proteins. Scheibel and co-workers review the application of these recombinant proteins in biomedical applications (article number 1704636). Polysaccharides are another important class of naturally occurring macromolecules. Their diversity in structure and function plays a very important role in nature and as materials for society. Wood itself can be considered a polysaccharide-based composite. It has served humanity throughout the entire history. However, wood is also a readily available hierarchical material that can be exploited as a large-scale biotemplate for functionalization at multiple length scales, as reviewed by Berglund and Burgert in article number 1704285. Moreover, they show how nanoscale structural control can be combined with the existing hierarchical structure of the wood template to generate novel materials. The main component of wood is cellulose, which is also the most abundant biopolymer on the planet. Cellulose, especially in its nano form is now found to be an excellent system to produce hierarchical optical materials with desired visual response, as shown by Vignolini and co-workers (article number 1704477) It is also a key component of multifunctional responsive materials, as reviewed by Godinho and co-workers (article number 1703655). A combination of the polysaccharides chitin and chitosan with proteins such as reflectin and pigments such as melanin is commonly used for dynamic camouflage in nature. These biomacromolecules can also find use in technology for the fabrication of certain voltage-gated devices and transistors, as reviewed by Kauts et al. in article number 1704917. Moving up the length scale, some nanomaterials such as iron oxide, gold, or silica nanoparticles, as well as liposomes, have found their way into clinical trials and drug formulations, e.g., as drug-delivery vehicles and contrast agents. To enhance their efficacy or performance, they are often designed in a way to mimic important features of cell surfaces or viruses, thus enhancing their circulation time and their specificity to certain targets. Rothen-Rutishauser and co-workers (article number 1704307) review the interaction of bioinspired and non-bioinspired clinically relevant nanomaterials with tissue. Moreover, the translocation of these nanomaterials across tissue barriers and their systemic fate and clearance from the body is discussed. Septiadi, Petri-Fink, and co-workers (article number 1704463) focus on a different aspect of nanoparticles. The interaction of nanoparticles with cells and their safe implementation into drugs and consumer products not only depends on the toxicity of the nanoparticles, but also on their influence on the mechanics of cells. In their Progress Report, they show how nanoparticles impair cell adhesion, cytoskeletal organization, and stiffness, and discuss the impact of particle-based nanomechanical measuring techniques, such as colloidal probe force microscopy and optical tweezers. Nature also offers an incredible variety of architectures made from inorganic materials. Diatoms alone feature more than 100 000 species with different morphologies and dimensions. Farinola and co-workers review the possibilities to manipulate these diatoms in order to produce hierarchical microstructures for a multitude of technological applications, e.g., by modifying their chemical composition (article number 1704289). In the context of inorganic bioinspired materials, Aizenberg's group reports a method to prepare hierarchical inorganic structures on large scales via colloidal co-assembly of colloidal particles and sol–gel precursors (article number 1706329). Living organisms can not only act as role model for novel bioinspired technologies, but can also be used directly to create structured materials, whereby the ability of the organisms to assemble into biofilms and hierarchical structures is key. Two Reviews in this special issue are dedicated to this topic. Van Opdenbosch and co-workers review the exciting possibilities to prepare materials with living microorganisms, whose self-assembly can be guided by light, magnetic fields, and other stimuli (article number 1703656). Meanwhile, Joshi and co-workers look at engineered living materials consisting of engineered bacteria and living composite materials (article number 1704847). Biological materials are also a source of inspiration for the architecture of synthetic materials. An example is mechanical gradients, which are used in nature to reduce strain mismatches in heterogeneous materials. Studard and co-workers develop a multimaterial 3D-printing platform to produce bioinspired elastomers with gradients of elastic modulus spanning three orders of magnitude (article number 1705808). Micrometer-scale surface structures are key elements in adhesive structures that mimic the gecko-foot or beetle toes. Much attention has been given to the hierarchical structure of adhesion devices. Now, Kizilkan and Gorb investigate the effect of the curvature of the backing layer that hosts the microstructure (article number 1704696). To this end, they produce flat, convex, and concave materials featuring mushroom-shaped and pillar-shaped adhesive microstructures and find that the adhesive forces are highest in the concave geometry. The surface curvature allows the adhesion to be tuned by a factor of 2, which implies new design rules for grippers and robots. Fiber-reinforced composites are used as lightweight and strong materials for a multitude of engineering applications, e.g., in the automotive and aerospace sector, as blades of wind turbines, as hulls for sporting boats, and for civil engineering structures such as bridges. Their outstanding mechanical properties arise from the reinforcing fibers, which have a diameter on the micrometer scale. However, fiber-reinforced composites can suffer micrometer-scale damage, e.g., due to impact events or overload. Many living organisms have developed means to sense damage to their tissue. Bruns and co-workers review approaches to mimic this ability in composites, i.e., to create self-reporting materials (article number 1705483). They indicate, through color changes or through sensor signals, that their structural health is in danger. Along similar lines, Weder, Schrettl, and co-workers report novel self-reporting poly(dimethylsiloxane)-based materials based on microencapsulated excimer-forming oligo(p-phenylene vinylene) (article number 1704603). These materials exhibit a ratiometric response to deformation, thereby self-calibrating themselves. On the macroscopic level, plants can serve as concept generators for the development of biomimetic actuators for architecture. Poppinga and co-workers review the state-of-the-art of plant movement, proposing principles and devices capable of producing complex and multidirectional shape changes with passive-hydraulic actuation (article number 1703653). In conclusion, this Special Issue showcases the fascinating research on bioinspired materials that many leading groups around the world pursue. We aim to give a balanced mix of review-type articles, research highlights, and original research from the leading experts in the field, covering aspects of the development of bioinspired materials across the different length scales. It is obvious that a Special Issue can only give a snapshot of such an active and large field of research, but we envisage that the readers will be inspired to tap into further, yet unexplored possibilities for the development of advanced materials based on biological concepts. The guest editors of this special issue work together in the Innovative Training Network Plant-inspired Materials and Surfaces – PlaMatSu and acknowledge funding from the European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 722842. Furthermore, N.B. is member of the National Center of Competence in Research (NCCR) Bio-Inspired Materials, and acknowledges financial support for this work by the Swiss National Science Foundation through the aforementioned NCCR and by grants No. PP00P2_144697 and PP00P2_172927. S.V. acknowledges the BBSRC David Phillips fellowship (BB/K014617/1) and the European Research Council (ERC-2014-STG H2020 639088). The editors thank all the contributing authors, many of which collaborate in PlaMatSu and the NCCR Bio-Inspired Materials. Special thanks go to Miguel Spuch-Calvar (Adolphe Merkle Institute) for the fabulous cover art.