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The Rise of Hierarchical Nanostructured Materials from Renewable Sources: Learning from Nature Francisco J. Martin-Martinez, Kai Jin, Diego López Barreiro, and Markus J. Buehler*

ACS Nano 2018.12:7425-7433. Downloaded from pubs.acs.org by UNIV OF SUNDERLAND on 08/28/18. For personal use only.

Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139, United States ABSTRACT: Mimicking Nature implies the use of bio-inspired hierarchical designs to manufacture nanostructured materials. Such materials should be produced from sustainable sources (e.g., biomass) and through simple processes that use mild conditions, enabling sustainable solutions. The combination of different types of nanomaterials and the implementation of different features at different length scales can provide synthetic hierarchical nanostructures that mimic natural materials, outperforming the properties of their constitutive building blocks. Taking recent developments in flow-assisted assembly of nanocellulose crystals as a starting point, we review the state of the art and provide future perspectives on the manufacture of hierarchical nanostructured materials from sustainable sources, assembly techniques, and potential applications. features and sustainability. The first bottleneck is that our technologies are still far from being truly able to mimic Nature, and thus, transferring the superior properties caused by nanoscale effects to the macroscale represents a great engineering challenge; namely, it is difficult to organize fundamental building blocks from the nanoscale into hierarchical structures with high levels of precision, while forestalling the appearance of defects that emerge from processing and assembly at larger scales. The second bottleneck is related to the sustainability of nanostructured hierarchical materials. It is of the utmost importance to develop a circular economy that keeps resources in use as long as possible, manufacturing materials in a facile, low-cost, and environmentally friendly manner. New synthetic and processing methods, such as the one reported by Mittal et al. in the July issue of ACS Nano for the assembly of nanocrystals, in combination with multiscale modeling and machine-learning techniques are a promising path to follow toward overcoming these bottlenecks.15 Beginning with recent progress in controlling the alignment of cellulose nanofibrils, in this Perspective, we discuss current scientific research and future improvements on utilizing biomass-derived nanostructured materials. Natural Nanostructured Hierarchical Materials: Learning from Nature How To Control Small Features. Natural materials consist of repetitive sequences made of simple building blocks that provide a wide variety of properties and functions, e.g., hydrophilic and hydrophobic segments of amino acids in silk, β-(1,4)-linked D-glucose units in cellulose, long-chain

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ature creates sophisticated materials with remarkable properties and multiple functions. These materials usually consist of simple molecular building blocks (e.g., amino acids, carbohydrates) whose behaviors are governed by their size, folding, assembly, interphases, and other nanoscale features.1 These finely defined hierarchical structures bridge macroscale properties with atomistic scale components. Many natural materials, such as cellulose in wood,2 chitin in crustaceans and insects,3,4 and fibroin in spider5 and silkworm silk, exhibit hierarchical structures made of nanofibrils (Figure 1).6 Other materials, such as nacre in pearls, present hierarchical structures in the form of brick-and-mortar architectures.7 These and other natural materials (e.g., bone) share the capacity to display multiple functions and have mechanical performances superior to those of their individual building blocks. Inspired by Nature, nanoscale science and nanotechnology, supramolecular chemistry, and self-assembly techniques have shown that indeed there is “plenty of room at the bottom” for the development of man-made hierarchical nanostructured materials with unique properties that differ from those of their bulk counterparts.2,8 Several factors, such as a high surface-tovolume ratio, quantum mechanical effects arising from a size comparable to the wavelengths of electrons and photons, and the capacity of nanostructures to distribute stress or to deflect cracks, all provide additional room for engineers to invent novel, complex bio-inspired nanoarchitectures with hierarchical designs and tailored properties that are guided by Nature.9−14 There are two primary bottlenecks in the development of nanostructured hierarchical materials: controlling nanoscale © 2018 American Chemical Society

Published: August 13, 2018 7425

DOI: 10.1021/acsnano.8b04379 ACS Nano 2018, 12, 7425−7433

Perspective

Cite This: ACS Nano 2018, 12, 7425−7433

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Figure 1. Overview of different hierarchical materials in Nature and how they go through different assembled structures from the macroscale down to the nanoscale. (A) Schematic representation of spider silk hierarchical structure for which silk fibroin is the main component. Adapted with permission from ref 8. Copyright 2018 Macmillan Publishing Limited. (B) Schematic representation of chitin hierarchical structure in the scaffold of crustaceous exoskeletons. Adapted with permission from ref 8. Copyright 2018 Macmillan Publishing Limited. (C) Schematic representation of wood hierarchical structure emphasizing the role of cellulose nanocrystals. Adapted with permission from ref 8. Copyright 2018 Macmillan Publishing Limited. (D) Schematic representation of bone hierarchical structure, with emphasis on hydroxyapatite crystals and collagen protein. Adapted with permission from ref 2. Copyright 2016 Macmillan Publishing Group.

inspiration for the development of smart nanostructured materials.21 For instance, chitin is arranged in a three-dimensional (3D) helicoid structural motif with important effects on both the mechanical and optical properties of the exoskeleton of arthropods and insects;3,4 nacre has a relatively simple brickwall-like architecture composed of polygonal tablets,22 and bone has a complex hierarchical structure23,24 with hydroxyapatite crystals embedded in a matrix of self-assembled individual tropocollagen molecules interacting through coordinated hydrogen bonds.25 Featuring a different multiscale arrangement, wood is organized in a hierarchical structure with highly oriented cellulose nanofibrils that helically wind along the longitudinal cell axis, controlling its mechanical anisotropy.13 Wood is mainly composed of three major molecules: cellulose, hemicellulose, and lignin (see Figure 1). Despite this simple chemical composition, it shows exceptional mechanical properties because of its hierarchical structure. Cellulose is arranged into crystalline ultraslim crystals with lateral dimensions of a few nanometers

New synthetic and processing methods, such as the one reported by Mittal et al. in the July issue of ACS Nano for the assembly of nanocrystals, in combination with multiscale modeling and machine-learning techniques are a promising path to follow toward overcoming these bottlenecks. polymers of (1,4)-β-N-acetylglucosamine in chitin, aragonite brick-and-mortar structures in nacre, and hydroxyapatite crystals in bone.16 In addition to their composition, these natural materials present special hierarchical designs that enable them to outperform their individual building blocks9,17 and that govern their deformation and fracture mechanisms.18−20 Natural materials such as chitin, nacre, and bone can be a source of 7426


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nanocellulose can be used for in situ softening of implants, cartilage replacements, drug-delivery systems, DNA extraction, antibacterial additives, wound healing, and tissue engineering.45,46 Hydrogels purely based on nanocellulose or in combination with other materials can be also applied to tissue engineering scaffolds, wound-healing materials, and drug-delivery systems.47 Ultralight, strong, and flexible foams and aerogels can be formed from nanocellulose by ice templating to generate iso- or anisotropic foams for implementation as scaffolds in biomedical applications as well as in energy storage systems.48 Also related to energy applications,49,50 nanocellulose has been used to manufacture high-strength electrodes, flexible devices,51 and supercapacitors.52 Moreover, the multichannel feature of wood has been utilized to develop sustainable water-treatment membranes.53 The strong cellulose fibrils can be also used as reinforcement agents for high-performance composite materials.54 It is expected that self-assembly55 and biomimetics56,57 will have great impact on developments related to nanocellulose. Chitin is the second most abundant natural polysaccharide on Earth, and it has similar functionalities to cellulose. Whereas cellulose is a structural material in the cell walls of plants, chitin is the main constituent of the cell walls of fungi, the exoskeletons of insects and crustaceans, and the radulae of mollusks. Although composite materials from self-assembled chitin nanofibers and microporous chitin materials have been produced,58 the potential of chitin has largely been underutilized due to poor solubility and processing difficulties. Future research could be directed toward two areas. The first area is the production of oriented nanofibrils with controlled anisotropy effects. New techniques, such as the microfluidic technique developed by Mittal et al., are a good approach in this regard.15 The second area is the combination of chitin fibers with other materials, such as chitin−nanocellulose blends, for the development of advanced composites with enhanced mechanical properties.59 Materials with biomass-derived nanostructures can not only mimic natural polymers but also offer the possibility of creating de novo advanced carbon materials. As shown in Figure 2, the processing of natural sources in combination with multiscale modeling techniques has the potential to produce a wide range of nanostructured materials. Hydrothermal conversion is one of the most promising techniques in this regard, offering the possibility to depolymerize biomass into simple building blocks and to combine them with other components to form composite materials with special chemical and physical properties.60,61 As a leader in this field, the Titirici group has applied hydrothermal conversion to produce carbon materials with different sizes and shapes as well as controllable morphologies and surface functional groups, e.g., morphology-controlled synthesis of carbonaceous nanospheres from sugar, glucose, cyclodextrins, fructose, sucrose, cellulose, and starch.33 The performances of these materials have shown promising results in photovoltaics, batteries, microbial fuel cells, and catalysis.62 Hydrothermal conversion holds great promise for the utilization of biomass resources in the manufacture of nanostructured hierarchical materials. Moreover, unlike fossil carbon materials, the use of biomass can provide doping elements to the resulting materials, conferring the materials with unique electronic properties. Research in this area should focus on understanding how key process parameters (e.g., temperature, pressure, reaction time, biomass/water ratio) affect the nanostructure and chemistry of the resulting carbon materials. Energy storage is the archetype of how overcoming the two aforementioned bottlenecks in nanostructured materials

and lengths of hundreds of nanometers. Hydrogen bonds stabilize the cellulose nanofibril bundles, whereas continuous covalent bonding along the nanofibrils provides outstanding stiffness and strength (∼150 GPa of modulus and ∼6 GPa of tensile strength).26,27 The amorphous matrix composed of a mixture of hemicellulose and lignin contributes to the toughness by introducing intermolecular sliding mechanisms that can dissipate energy under stress.28−30 In silk, the excellent mechanical properties originate from its protein sequence, which triggers a self-assembly process that results in a highly ordered nanostructure that is stabilized through noncovalent interactions, i.e., hydrogen bonds and electrostatic interactions. For many years, silk has been considered the gold standard of highly organized lightweight biopolymers, due to its extremely high strength and toughness. The building blocks (i.e., amino acids) are confined to a critical nanoscale with β-sheet nanocrystals of a few nanometers (2−5 nm) that optimize strength, stiffness, and toughness through a consequent dissipative molecular stick−slip deformation that would not be possible with larger nanocrystals.31 Overall, nanoconfinement, nanofibril orientation, helicoidal stacking, and nanocrystal alignment are common features to most of the materials that we discussed. Understanding the mechanisms that govern these and other natural materials will help us in designing a new generation of processing techniques and nanostructured materials with superior mechanical performance, stimuli-responsive features, self-healing mechanisms, or slow crack-propagation behaviors. Biomass-Derived Materials: Toward a Circular Economy. Mimicking Nature in materials science goes beyond hierarchical designs of nanostructured materials to include the development of more efficient and sustainable pathways to produce the materials. Sustainable production of materials will move toward a circular economy that mimics the well-integrated cycles that Nature has developed over millions of years to reuse scarce resources efficiently. Although the utilization of biomass has typically focused on biofuel research, it has arisen as a widely available source for the synthesis of carbon materials.32,33 Many building blocks of interest (e.g., cellulose, lignin, chitin, amino acids) can be obtained from the depolymerization of biomass. The development of advanced biomassprocessing technologies is a great challenge34 that has impact in many different areas, such as energy storage,35,36 catalysis, civil infrastructure, and CO2 capture. Thus far, biomass-derived materials have been generated from a wide range of sources including bacterial cellulose, lignin, cornstalk, corn starch, sweet potato, peanut shells, pinecone hull, banana skins, cherry stones, and bamboo chopsticks.37,38 Wood (i.e., lignocellulosic biomass) is of special interest because of the chemical composition of its fundamental building blocks.39 There are two approaches for the utilization of wood. On the one hand, the hierarchical cellular structure of wood itself is a great platform for engineering applications. Wood is a lightweight material that can rival steel and other engineering materials in specific modulus and strength. On the other hand, technological advances in the past decades have facilitated the depolymerization of wood into its building blocks (cellulose, hemicellulose, and lignin) and its implementation for different applications. Cellulose can be isolated into a one-dimensional (1D) crystalline material referred to as nanocellulose,40−43 which can be classified into cellulose nanocrystals and cellulose nanofibers. The potential applications of cellulose nanomaterials are countless.44 In biomedicine, 7427


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Figure 2. Schematic representation of some examples of biomass sources to be transformed into tailored nanostructured materials through different processing techniques in combination with predictive multiscale modeling: (A) manure, (B) microalgae, (C) wood, (D) sewage sludge, (E) crustaceous scaffolds. (F) Scanning electron microscope (SEM) micrograph of silver−carbon nanostructured composites. Reprinted with permission from ref 61. Copyright 2007 John Wiley & Sons, Inc. (G) Transmission electron microscope (TEM) micrograph of Pt-nanoparticle-loaded coating carbon nanofibers. Reprinted with permission from ref 60. Copyright 2006 Royal Society of Chemistry. (H) SEM micrograph of sucrose-derived carbon nanospheres. Reprinted with permission from ref 62. Copyright 2012 Royal Society of Chemistry. (I) SEM micrograph of furfural-derived carbon nanospheres. Reprinted with permission from ref 62. Copyright 2012 Royal Society of Chemistry. (J) SEM micrograph of microporous chitin. Reprinted with permission from ref 58. Copyright 2015 Royal Society of Chemistry. (K) SEM micrograph of a freeze-dried bacterial cellulose sample. Reprinted with permission from ref 43. Copyright 2009 Royal Society of Chemistry. (L) SEM micrograph of fructose-derived carbon nanospheres. Reprinted with permission from ref 62. Copyright 2012 Royal Society of Chemistry.

of electrons or from electrostatic interactions, among others. Spinning techniques mimic spiders’ mechanism to produce 1D nanofibrils. More complex mechanisms that incorporate electric or magnetic fields can lead to the formation of 2D materials such as membranes and nanopapers. All these approaches provide avenues for the replication and expansion of the properties of selfassembled biomaterials such as chitin, wood, or silk, to yield lightweight, biocompatible, and mechanically resistant novel biomaterials with unique electrical, thermal, or optical properties. The ability to combine different building blocks into complex architectures has opened unprecedented opportunities in materials science and engineering, with impacts in all areas of human life, including biomedicine,72,73 infrastructure,74 hydrogen production,75 water desalination,76 and even preservation of cultural heritage.77 Many of these nanostructured materials need good mechanical performance in addition to properties specific to their area of application. Whether they are biomaterials, polymer-based materials, inorganic nanoparticles, carbon nanomaterials, or a combination thereof, the implementation of bio-inspired hierarchical designs that mimic natural materials will improve their durability and performance under working conditions.

(capacity to control nanoscale features and using sustainable resources) can greatly impact the economic success of a sector. There is a great deal of attention devoted to the development of nanostructured materials to replace conventional materials63 for hydrogen storage systems,64 supercapacitors,65 Li/ion batteries,66,67 biofuel cells,68 and redox flow batteries.66 Coming developments are expected to provide high specific surface area, controllable porosity, high electronic conductivity, better performing electroactive sites, high thermal stability,65 and engineered water pathways in electrodes.69,70 Producing those electrodes with controlled porosity and surface chemistry from biomass sources through hydrothermal conversion can improve the electron transfer due to the effect of nitrogen-doping, for example.71

Materials with biomass-derived nanostructures can not only mimic natural polymers but also offer the possibility of creating de novo advanced carbon materials. Multiscale Control of Assembly and Self-Organization. Current advances in areas such as nanotechnology, characterization of materials, microfluidics, and synthesis techniques have enabled control of the arrangement of atoms and molecules at the nanoscale to produce nanostructured materials with 1D, 2D, and 3D structures that incorporate oriented nanofibrils, nanocrystals, and other geometrical features at the nanoscale and have properties arising from the nanoconfinement

The combination of different building blocks into complex architectures has opened unprecedented opportunities in materials science and engineering, with impact in all areas of human life. 7428


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Figure 3. (A) Illustration of the silkworm spinning process in the spinning gland. (B) Bio-inspired spinning process that assembles nematic silk microfibril solution into regenerated silk fibers. The inset is a scanning electron microscope (SEM) image of the fiber cross section showing that the silk microfibrils are well aligned. (C) Schematic of how the silk microfibrils are aligned under the shear/stress elongation. Images A−C are adapted with permission from ref 78. Copyright 2017 Macmillan Publishers Limited. (D) Double flow-focusing channel used for cellulose nanofibril assembly. Hydrodynamic and electrostatic interactions at different positions are arranged to maximize the nanofibril alignment. (E) Scanning electron microscope image of the fiber surface and cross sections, showing the aligned nanofibrils. Images D and E are adapted from ref 15. Copyright 2018 American Chemical Society.

Printable inks composed of cellulose fibrils have been developed and applied to build 3D structures, such as all-cellulose hydrogels or composite structures where cellulose fibrils work as mechanical reinforcement.80−83 As ink is extruded from the printer syringe, the cellulose fibrils experience hydrodynamic effects that force the fibrils to align along the printing direction, resulting in anisotropic printed structures with higher mechanical stability along that direction. The anisotropy of the printed material opens up possibilities for creating patterned structures with various responses. In work performed by Jennifer Lewis’ group,81 various patterns were printed with the anisotropic swelling properties of the printed fibrils. The structures achieved moisture-induced responsive deformation, which added another dimension of deformation. Future research in microfluidic or 3D printing of robust fibers could focus on the various methods by which the properties of the extruded fibers can be tuned, including selecting the dimensions of the nanofibrils, which is a fundamental factor for controlling the macroscale properties,84 and adjusting the degree of repulsion in the nanofibrils suspension, for example, by varying the degree of cellulose oxidization and the flow velocity. Printing hybrid, gradient structures with varying mechanical properties is also an area worth exploring. Although the cellulose alignment within natural wood has inspired the development of techniques for aligning fibrils, the wood cell wall itself is already an existing fibril-aligned structure. Different from the approach of regenerating cellulose fibers from nanofibrils, Hu et al. generated cellulose-aligned materials directly from wood.85 After most of the soft matrix molecules composed of lignin and hemicellulose was extracted, the resulting wood was further compressed into densified material to maximize the interfibril interactions between the cellulose fibrils. The resulting material featured a modulus above 50 GPa and strength of ca. 600 MPa. Although these numbers are lower than the modulus and strength of all-cellulose materials because of the existence of residue hemicellulose and cellulose, this technique tends to be easier to realize and is more suitable for bulk production. Due to the anisotropy from the alignment of nanocellulose fibrils, the materials developed from this technique

An area of great interest is the development of dense macroscopic fibers from nanocellulose fibrils; such fibers can synergistically maximize stiffness and strength, the same way silk, chitin, or cellulose fibers do in Nature. Various techniques are being developed in this regard, including wet and dry spinning techniques. All these processes resemble how spiders convert an aqueous solution of short amino acid chains into a robust silk fiber. This process is based on the application of shear stress to stabilize interactions within nanofibrils so that they self-assemble into aligned fibers (Figure 3A−C).78 The mechanical properties of the resulting fibers appeared to be highly dependent on the extrusion and reeling speeds. Although this approach has made it possible to generate silk in the lab that surpasses the mechanical properties of natural silk,78 the mechanical properties of the nanocellulose fibers are usually far from the theoretical limits of crystalline cellulose. This discrepancy calls for new techniques to enhance the alignment of the cellulose nanofibrils during the spinning process. One obstacle in forming perfectly aligned fibrils is the colloidal gelation of the nanofibrils, which reduces the mobility of the fibrils under flow. Spiders vary the ionic concentration in the spinning solution to prevent this, and this behavior has served as inspiration for the development of microfluidic setups for cellulose.15,79 Soderberg et al. proposed combining electrostatic and hydrodynamic interactions to maximize the fibril alignment. The surface of cellulose fibrils was oxidized to introduce carboxylic groups, which introduced electrical repulsions between the fibrils. As a result, the fibrils were free to move and to rotate before undergoing an extensional flow that aligned the fibrils. A second stage of extensional flow was incorporated before the final settling down, in order to prevent disorder because of the Brownian motion. Eventually, the fibrils were fixed through colloidal gelation by removing the electrical repulsion through protonation of the carboxylic groups (Figure 3D,E). The resulting fibrils feature a modulus up to 86 GPa and strength above 1 GPa. As additive manufacturing emerges as an advanced technique for the fast and reliable fabrication of hierarchical structures, spinning and self-assembly are finding roles in this area. 7429


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reactions in many biomolecular systems.99 These approaches enable the modeling of reactive biomolecular systems with a reasonable computational effort while providing the necessary accuracy. In addition, machine learning is a rising instrumental tool for designing new molecules, materials, and composites for future engineering applications. Machine learning enables computers to learn from past experiences to detect patterns that are hard to discern in large, complex data sets. As a result, machine learning is increasingly being used in materials science, rather than the finite element method or other traditional evaluation models, to speed up simulations and to design new materials.100

are also useful for directional thermal conduction and mass transportation.86,87 Multiscale Modeling and Computational Challenges: Materials by Design. The material-by-design paradigm is expected to guide coming developments of hierarchical nanostructured materials, as it has been implemented for biomaterials, proteins, polymers, and nanomaterials. This paradigm synergistically integrates theoretical design at the atomic level; modeling of materials at the nano-meso-microscale; and additive manufacturing, synthetic chemistry, and process engineering at the macroscale to develop materials according to specific rational designs. Recent progress in controlling the alignment of cellulose nanofibrils and future improvements in utilizing biomass materials also open fundamental questions and offer the opportunity to realize model designs experimentally. Multiscale modeling provides deep understanding of the structure−function and structure−property relationships of materials. Multiscale modeling uses quantum mechanics calculations, like those provided by density functional theory, to describe the electronic structure of individual building blocks as well as larger scale models to understand the structure of the materials up to the continuum level. In the case of biomassderived materials such as cellulose, silk, or chitin, multiscale modeling also aids in the development of better synthesis and processing techniques and depolymerization strategies. Lignocellulosic biomass is a good example of where multiscale modeling is able to describe all key fundamental features of such hierarchical materials at different length scales.88 Multiscale modeling has made it possible to understand the roles that the different components of wood and their spatial arrangements play in determining the mechanical strength of lignocellulosic biomass. Multiscale modeling also unlocked the role of hydrogenbonding interactions of cellulose−hemicellulose systems and the covalent bond linkages of hemicellulose−lignin systems,89 as well as those related to the lignin−carbohydrate complex,90 in which the nature of the polysaccharide matrix induces selective binding with preferred orientations, affecting the architecture of the hemicellulose in the cell wall.91 New computational tools have made it possible to build virtual cellulose− hemicellulose networks by stochastic self-assembly.92 Standalone models for lignin are needed to understand its structure and its role in lignocellulosic wood. New force fields,93 with special attention paid to b-O-4 linkages, open new possibilities for computational simulations of lignin and lignocellulosic biomass. In addition, CHARMM force fields have been applied to study the influence of hydrogen-bonding assembly of cellulose and lignin.94 The conversion of biomass-derived materials into usable materials, such as carbon fibers, membranes, or hydrogels, can greatly benefit from the development of accurate computational models. In the case of lignocellulosic biomass, the development of tailored reactive force fields (ReaxFF)95 or finite element models are research efforts worth mentioning.96 In the case of silk, atomistic and coarse-grained molecular dynamics simulations have been used in combination with experiments to understand how processing conditions and design parameters control the anisotropy and self-assembly of fibers upon spinning.97,98 The complexity of hierarchical structures along different large scales, together with computational limitations, requires the implementation of new methodologies in the field. Combined quantum mechanics/molecular mechanics (QM/MM) approaches have become the method of choice for modeling

CONCLUSIONS AND OUTLOOK The creation of nanostructured hierarchical materials with bioinspired and biomimetic designs will provide new sustainable functional materials. Wood, chitin, and silk are examples of natural materials that possess multiple functions with superior mechanical properties mainly attributed to their hierarchical structure of nanofibrils, which efficiently self-assemble under mild conditions. Current material production techniques impose the restriction that both macro- and nanoscales be manipulated simultaneously, which is expected to change with coming advanced nanotechnologies. Using computational modeling to understand and to mimic the assembly and structural features of these materials enables multiscale, rational material design strategies to optimize structure−property− function relationships. Harnessing control over self-assembly processes and understanding the intricate connection between hierarchical structure and macroscopic properties expands the materials space domain to manufacture new bio-inspired nanostructured materials. We can aspire to go beyond the pure imitation of Nature, creating novel properties through the combination of natural and/or non-natural building blocks. Some approaches in this direction have already been undertaken in combination with microfluidic techniques to obtain nanocellulose macroscale fibers,15 or using solvent−biopolymer interactions for the development of robust silk hydrogels101 and fibers.98 Bottom-up and top-down approaches to control the macroscopic shape and nanoscale orientation of silk simultaneously102 and control self-assembly of short peptides into semiconductors103 are also promising strategies. Furthermore, creating composite materials that combine the properties of two or more of the natural biopolymers is also an innovative approach to obtain biomaterials with emerging properties, e.g., combining silk and nanocellulose through microfluidic processing to create mechanically robust and bioactive materials15 or using recombinant DNA techniques to combine silk and elastin domain into silk−elastin-like proteins to create novel protein-based biopolymers that present unique responses to changes in temperature, pH, or biological triggers.104 More complex processing routes (e.g., hydrothermal conversion) can turn widely available resources like wood or chitin into novel carbon-based materials. Such transformations have been achieved, for instance, by the thermal treatment of chitin to obtain carbon nanoparticles105 that can heat significantly upon laser irradiation106 and could be used as stimuli receptors for thermoresponsive materials or by carbonizing silk fabrics to yield conductive materials that preserve the nanostructure from silk but with high conductivity that enables their use in highly sensitive wearable sensors.107 The need for greener chemical processes imposes an additional requirement on the development of novel materials. Materials should be obtained from sustainable resources, nontoxic, 7430


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(4) Fabritius, H.-O.; Ziegler, A.; Friák, M.; Nikolov, S.; Huber, J.; Seidl, B. H. M.; Ruangchai, S.; Alagboso, F. I.; Karsten, S.; Lu, J.; Janus, A. M.; Petrov, M.; Zhu, L. F.; Hemzalová, P.; Hild, S.; Raabe, D.; Neugebauer, J. Functional Adaptation of Crustacean Exoskeletal Elements through Structural and Compositional Diversity: A Combined Experimental and Theoretical Study. Bioinspir. Biomim. 2016, 11, 055006. (5) Tao, H.; Kaplan, D. L.; Omenetto, F. G. Silk Materials - A Road to Sustainable High Technology. Adv. Mater. 2012, 24, 2824−2837. (6) Neville, A. C. Biology of Fibrous Composites: Development beyond the Cell Membrane; Cambridge University Press, 1993. (7) Gao, H.-L.; Chen, S.-M.; Mao, L.-B.; Song, Z.-Q.; Yao, H.-B.; Cölfen, H.; Luo, X.-S.; Zhang, F.; Pan, Z.; Meng, Y.-F.; Ni, Y.; Yu, S.H. Mass Production of Bulk Artificial Nacre with Excellent Mechanical Properties. Nat. Commun. 2017, 8, 287. (8) Ling, S.; Kaplan, D. L.; Buehler, M. J. Nanofibrils in Nature and Materials Engineering. Nat. Rev. Mater. 2018, 3, 18016. (9) Sun, H.; Luo, Q.; Hou, C.; Liu, J. Nanostructures Based on Protein Self-Assembly: From Hierarchical Construction to Bioinspired Materials. Nano Today 2017, 14, 16−41. (10) Buehler, M. J. Large-Scale Hierarchical Molecular Modeling of Nanostructured Biological Materials. J. Comput. Theor. Nanosci. 2006, 3, 603−623. (11) Buehler, M. J.; Keten, S.; Ackbarow, T. Theoretical and Computational Hierarchical Nanomechanics of Protein Materials: Deformation and Fracture. Prog. Mater. Sci. 2008, 53, 1101−1241. (12) Pieters, B. J. G. E.; van Eldijk, M. B.; Nolte, R. J. M.; Mecinović, J. Natural Supramolecular Protein Assemblies. Chem. Soc. Rev. 2016, 45, 24−39. (13) Fratzl, P.; Weinkamer, R. Nature’s Hierarchical Materials. Prog. Mater. Sci. 2007, 52, 1263−1334. (14) Ren, Z.; Guo, Y.; Liu, C.-H.; Gao, P.-X. Hierarchically Nanostructured Materials for Sustainable Environmental Applications. Front. Chem. 2013, 1, 1−22. (15) Mittal, N.; Ansari, F.; Gowda. V, V.; Brouzet, C.; Chen, P.; Larsson, P. T.; Roth, S. V.; Lundell, F.; Wågberg, L.; Kotov, N. A.; Söderberg, L. D. Multiscale Control of Nanocellulose Assembly: Transferring Remarkable Nanoscale Fibril Mechanics to Macroscale Fibers. ACS Nano 2018, 12, 6378−6388. (16) Buehler, M. J.; Yung, Y. C. Deformation and Failure of Protein Materials in Physiologically Extreme Conditions and Disease. Nat. Mater. 2009, 8, 175−188. (17) Roth, W. J.; Gil, B.; Makowski, W.; Marszalek, B.; Eliásǒ vá, P. Layer Like Porous Materials with Hierarchical Structure. Chem. Soc. Rev. 2016, 45, 3400−3438. (18) Dunlop, J. W. C.; Weinkamer, R.; Fratzl, P. Artful Interfaces within Biological Materials. Mater. Mater. Today 2011, 14, 70−78. (19) Barthelat, F. Architectured Materials in Engineering and Biology: Fabrication, Structure, Mechanics and Performance. Int. Mater. Rev. 2015, 60, 413−430. (20) Spivak, D. I.; Giesa, T.; Wood, E.; Buehler, M. J. Category Theoretic Analysis of Hierarchical Protein Materials and Social Networks. PLoS One 2011, 6, e23911. (21) Ragni, R.; Cicco, S. R.; Vona, D.; Farinola, G. M. Multiple Routes to Smart Nanostructured Materials from Diatom Microalgae: A Chemical Perspective. Adv. Mater. 2018, 30, 1704289. (22) Barthelat, F.; Tang, H.; Zavattieri, P. D.; Li, C. M.; Espinosa, H. D. On the Mechanics of Mother-of-Pearl: A Key Feature in the Material Hierarchical Structure. J. Mech. Phys. Solids 2007, 55, 306− 337. (23) Rho, J.-Y.; Kuhn-Spearing, L.; Zioupos, P. Mechanical Properties and the Hierarchical Structure of Bone. Med. Eng. Phys. 1998, 20, 92−102. (24) Weiner, S.; Wagner, H. D. THE MATERIAL BONE: Structure-Mechanical Function Relations. Annu. Rev. Mater. Sci. 1998, 28, 271−298. (25) Buehler, M. J. Nature Designs Tough Collagen: Explaining the Nanostructure of Collagen Fibrils. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 12285−12290.

and, especially in the biomedical sector, biocompatible. These conditions provide significant room for improvement, as many of the processes for converting bioresources like wood or silk into nanostructured materials make use of toxic chemical solvents and harsh processing conditions to depolymerize and to convert those feedstocks into usable materials. So far, the conditions that processes be sustainable, nontoxic, and biocompatible are not transferable to scaled-up production, which is a significant hindrance in the use of these feedstocks for commercialization of novel materials. Further improvements in a scaled-up process are needed to make these materials suitable for real applications. Finally, it is important to note the great potential that computational modeling holds for all these challenges. Modeling can be applied to unlock the structure−function relationships of natural materials, to assist in the development of synthetic materials, and to discover advanced processing routes that maximize the properties of the resulting products. Developing scalable quantum mechanics calculation codes, accurate force fields for atomistic simulations, and advanced algorithms and theories that build on and combine the existing theories will improve prediction capabilities of specific functional outcomes. High-throughput computational screening and, more importantly, new artificial intelligence and machine-learning algorithms applied to the field of materials discovery may provide unprecedented methodologies for the computational design of materials as well as novel, more effective routes to improve the validation of nanostructured materials screening and design. The combination of bio-inspiration, multiscale modeling, highthroughput supercomputing, machine learning, nanotechnology, microfluidics, additive manufacturing, and processes engineering is expected to generate an increase in hierarchical nanostructured materials from renewable sources in the years to come. Mimicking Nature offers numerous advantages in terms of designing and manufacturing nanostructured materials, and a combination of the above-mentioned techniques has the potential to face most of the challenges associated with this goal.

ACKNOWLEDGMENTS The authors acknowledge support from the US Department of Defense − Office of Naval Research (N00014-16-1-233), and US Department of Defense − Air Force Office of Scientific Research MURI (FA9550-15-1-0514). Additional support from NIH U01 HS 4976 is acknowledged. AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. ORCID

Markus J. Buehler: 0000-0002-4173-9659 Notes

The authors declare no competing financial interest.

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