Introduction

Life thrives in every environment on Earth, from the harshest deserts to the crushing pressure of the ocean’s depths. Within the constraints of the material building blocks of life, hundreds of millions of years of evolution by natural selection have produced an extraordinary diversity of functional solutions. It is, therefore, no surprise that biology offers solutions to many of the problems we face today. The need to find sustainable solutions to existentially significant challenges, such as climate change, the energy crisis, plastic pollution, biodiversity declines, antimicrobial resistance, and food insecurity, has fueled rapid growth in biomimetic and bioinspired materials and technologies. These span many fields1, such as advanced manufacturing2,3; photonics and electronics4,5,6; robotics7, and biomedical and energy applications8,9. But despite this progress, we have yet to discover, fully understand and take advantage of nature’s material design principles10, and we are still far from achieving precision nanomanufacturing of even the simplest organisms, such as diatoms11. Current frontiers in materials innovation are concerned with many of the properties that are inherent to biological materials, such as sustainability, self-assembly, multifunctionality, responsiveness, self-repair, and replication12. Drawing from nature’s designs has therefore become more than a trend - it is arguably an imperative.

There is now a large and growing literature on the principles and practice of bioinspired design13,14,15,16,17,18, and numerous reviews of recent advances in types of bioinspired materials, e.g.,2,7,12,19,20,21,22,23,24,25,26,27. Here our goal is not to duplicate these efforts, but to identify key challenges to the effective design and development of bioinformed materials more generally, and ways to address those challenges. We begin by briefly outlining the overarching goal of bioinformed materials design in the context of sustainability. We then identify current challenges and promising approaches in three key areas: 1) accessing and harnessing biological information; 2) multifunctionality; and 3) designing and manufacturing bioinformed materials. We outline guiding principles for practitioners in the field, including researchers, designers, engineers and industry professionals, highlighting key examples to illustrate these principles.

From bioinspired to bioinformed

The natural functions and properties of biological materials can inform and even reimagine synthetic materials23,28. However, the perceived value of biomimetic and bioinspired approaches is often undermined by the prevalence of superficial biological analogy29. Previous studies have emphasized the importance of defining and differentiating between biomimetic and bioinspired approaches30. The terms distinguish respectively “between attempting to replicate a biological property or function versus applying a principle or process that underpins a biological system”15. In practice, there is a continuum in the degree of similarity to biological form or function; both approaches require us to understand and distil essential properties of complex biological systems. We argue that first and foremost, these approaches must be bioinformed. The term bioinformed describes a design approach that is informed by detailed and accurate information on biological systems or processes and makes a clear distinction from approaches that are based on superficial, figurative or one-dimensional analogy15. A bioinformed design approach considers multiple properties and functions of biological materials, which are also desirable in synthetic materials, to create a product that meets multiple design criteria. An approach that considers multiple properties and functions of biological materials, systems or processes has been repeatedly advocated in the literature on biomimetic and bioinspired design31,32,33,34, but has not been conceptually differentiated. We therefore adopt the term bioinformed to make clear this conceptual distinction and argue for the utility of such an approach to materials innovation.

Sustainable materials for a circular economy

Sustainability is a growing imperative for future materials, and an area with significant potential to draw on biological solutions. However, sustainability is a broad concept that has different meanings from human and ecological perspectives. From a human perspective, sustainability, or more specifically sustainable development, has been defined by the United Nations Brundtland Commission as “meeting the needs of the present without compromising the ability of future generations to meet their own needs”35, and is operationalized in the United Nations’ 17 Sustainability Goals36. From an ecological perspective, sustainability describes the ability of biological systems to remain healthy, diverse, and productive over time. Thus, sustainability is a concept that applies to higher levels of biological organization, such as ecosystems, rather than to individual species.

In ecosystems, species perform different functional roles; for example, primary producers such as plants use solar energy to synthesize organic compounds, which are then consumed by herbivores; and detritivores consume and breakdown waste material from consumers, which then provides nutrients for primary producers. In a similar way, the sustainability of materials should ideally encompass the entire cycle of an engineered material in a systems context (Fig. 1). This is a core requirement of a circular economy37, defined by the World Economic Forum as “an industrial system that is restorative or regenerative by intention and design”38. Under a circular economy model, materials and products are designed for durability, reuse, remanufacturing, and recycling in contrast to the current linear take-make-consume-discard industrial system. There are clear analogies between ecosystems and a sustainable, circular economy industrial system, with substantial scope for bioinformed enhancement of materials at different stages of the materials life cycle, from raw materials to manufacture and end-of-life management (Fig. 1). For example, there are extensive efforts to develop sustainable and biodegradable biopolymers to replace petrochemical polymers and to design for disassembly through the use of enzymes39,40. Embedding a holistic, entire lifecycle view into materials design represents one of the greatest challenges for the future of bioinformed materials, beyond the commercial requirements that such materials are economical at the required scale and lend themselves to mass manufacturing.

Fig. 1: Materials and surfaces in nature are adaptive, biodegradable, multifunctional, self-assembling, self-cleaning, and self-repairing.
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The five images within the bioinformed cycle show examples of materials/surfaces exhibiting these features (self-repairing not shown) and describe bioinspired materials and technologies with these properties. Bioinformed materials should ideally exist within a circular bioinformed material lifecycle to achieve sustainability. Such materials can be designed and manufactured to be biodegradable using recycled materials, they can then be distributed using methods which reduce environmental waste, and finally at the end of life, materials can be recycled or reused. All images from unsplash.com.

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Accessing biological information

At first glance, design practitioners have access to a vast biological literature that seems to provide unlimited possibilities to draw from. In practice, however, translating these biological concepts to other disciplines is challenging17,41. Practitioners are often overwhelmed when confronting the knowledge gap required to understand a different field and translate it into their disciplinary context15,42. This has spurred the development of databases, such as Ask Nature43 and calls to expand such databases to generate a Biological Information System44. While these databases are undoubtedly valuable, they can help to perpetuate the use of limited model biological systems and an overly simplistic understanding of structure-function relationships. They often ignore the myriad variations on a theme that enable organisms to adapt to diverse and specific biotic and abiotic environments, and the multiple competing functions that these adaptations accommodate45. For example, the tokay gecko (Gecko gecko) completely dominates the literature as a model for gecko-like adhesives15, yet this unusually large species is only one of over 1000 species of gecko, each of which provides a unique evolutionary solution to surface attachment in the context of their own environmental niche46. Use of this single-species model therefore restricts our ability to develop bioinformed adhesive materials across a broad range of applications and contexts.

An alternative source of biological information is publicly available curated databases that aim to systematically document aspects of biological diversity. For example, Yan et al.47 reported the construction of a large nanomaterial database containing annotated nanostructures for 705 unique nanomaterials covering 11 material types (http://www.pubvinas.com/). Such databases provide important insight into the evolutionary diversity of a desired material; for instance, Arakawa et al.48 provide a silkomics database documenting the genetic diversity of spider silks in over 1000 species. In addition, natural history collections have become increasingly digitized and provide a rich source of information on georeferenced biological specimens. These collections implicitly contain environmental information through georeferencing. To connect structures to the environment in which they occur, structural, material, or trait information, could be integrated into georeferenced natural history collections. This is already occurring in an ad-hoc fashion (e.g. publicly available computed tomography (CT) and micro-CT scans linked to specimens)49,50, and there are growing efforts towards many forms of high-throughput trait characterization51,52,53. We envisage that such efforts could be systematically extended to include imaging at different length scales, and other forms of material characterization. Equally, existing information, which is often stored haphazardly, needs to be collated and curated within centralized, publicly accessible repositories.

Leveraging biological diversity

While curated, annotated and georeferenced databases can improve access to accurate biological information and link it to specific environments, we must also consider how this information is integrated into the design process. Conventional bioinspired materials design focuses on a particular biological example or material property as the basis for narrow optimization of a specific property or function. We emphasize that this conventional approach should be broadened to more effectively leverage biodiversity54. This could be approached in several ways. First, properties or functions of biological materials could be investigated across multiple organisms to reveal how these characteristics vary in different environments (Box 1) and to identify fundamental design principles shared by many organisms. Comparison of closely related species with shared evolutionary, developmental, and material constraints can reveal the specific modifications required to achieve different functional solutions in different environments55. For example, major ampullate (MA) silks from Argiope spiders, commonly found in tropical grasslands, appear to be more resistant to temperature and humidity stress than those spun by Leucauge species from tropical forests56. Conversely, comparison of distantly related species can reveal general underlying principles or convergent solutions to a problem. For example, the eggs of the leaf insect (Phyllium philippinicum) and the seeds of the ivy gourd (Coccinia grandis) have different adhesive structures, but these share certain design features57. The presence of adhesive fibrillar structures in both these models suggests that fiber reinforcement is an effective solution to surface attachment across different biological and ecological contexts58.

Second, properties or functions in different taxa can be combined to produce hybrid multifunctional materials; for example, the development of spider silk and bacterial cellulose hybrid ‘smart’ switches and pores for multiple applications. Third, different biological models or sources of biological information can inform multiple stages of the material life cycle. For instance, the design of self-cleaning materials can be informed by hydrophobic surfaces found in nature, whilst the packaging of such products can be informed by other solutions featuring high degrees of biodegradability. This diversity-driven approach is more challenging than the conventional approach but will be necessary to design bioinformed materials for a circular economy.

Multifunctionality

Understanding the structure-function relationship in biology is essential to bioinformed design and one of the most significant challenges faced by biologists and materials scientists alike. Multifunctionality is a hallmark of biological materials, which commonly achieve diverse functional solutions through variation in structure rather than through variation in material composition22,24. To achieve a diversity of functions, biological structures are often highly complex, composite or modular, and hierarchical (i.e., with different properties at different length scales; Fig. 2)24. Additionally, there is rarely a one-to-one correspondence between structure and function in biology. One domain of a hierarchical structure can serve many functions, and organisms have evolved a remarkable diversity of solutions to similar functional problems (Fig. 3). For example, each of the close to 100,000 species of marine diatoms has developed its own unique hierarchically nanostructured silica shell as an elegant solution to solve its mechanical, molecular transport and optical problems59,60. This is achieved under physiologically compatible and environmentally benign conditions using minimal energy and producing minimal waste. Even in well studied taxa like birds, each of the approximately 10,000 species has its own unique combination of feather coloration and detailed feather arrangement to meet the organism’s aerodynamic, thermal, sensory and communication needs61. As with diatoms, this reflects the need for organisms to simultaneously optimize multiple functional requirements, together with specific combinations of ecological and evolutionary processes that generate diversity in biological systems. Importantly, the observed variation within a taxonomic group (e.g., diatoms) is limited by evolutionary and developmental constraints, and these design constraints are very different from those for synthetic materials. Yet efforts to characterize biological materials often focus on single characteristics (e.g., optical, thermal, or mechanical properties), in single species, with little knowledge of such constraints or adaptive value within their environment.

Fig. 2: Structures producing green coloration in some butterflies - an example of complex, modular, and hierarchical biological structures.
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a High magnification image of a green wing scale from the butterfly Thecla opisena (image by B. Wilts adapted from ref. 93). Green coloration is produced by discrete chitin domains. b Scanning electron micrograph (SEM) of the wing scale showing the structure of the domains. Each domain comprises a porous network-like structure that closely resembles the single gyroid (a highly ordered 3D photonic nanostructure). c A simulated unit cell of the gyroid showing the two intertwined channels (blue and yellow surfaces) and the two ‘srs’ nets (a type of 3D network structure) embedded within each channel (red and green graphs). In the butterfly, one of these channels is filled with chitin allowing the nanostructure to operate as photonic crystals. d A magnified SEM micrograph of the wing scale with the upper lamina partially removed showing a closer view of the gyroid domains and their attachment locations on the lower lamina. The inset is a photograph of a male Thecla opisena (image by K. Garwood adapted with permission from butterflycatalogs.com).

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Fig. 3: Examples of structural diversity found in nature.
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Biological materials and structure such as diatom shells (a, b, c), shark skin (d, e, f), moth antennae (g, h, i), and compound eyes (j, k, l) often vary in structure across species depending on ecological context. Diatom shell images adapted from ref. 94, CC BY 4.0. Shark skin images adapted from ref. 95, CC BY 4.0. Beetle antennae images are in the public domain from flickr.com by T. Olson produced as part of the Insects Unlocked Project at the University of Texas at Austin. Fly compound eye images are in the public domain from flickr.com by Sam Droege produced as part of the USGS Native Bee Inventory and Monitoring Program at the Eastern Ecological Science Center.

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An additional complication is that structure-function relationships in biology may not always be obvious even when analyzed at the nanoscale, especially as the function of a material is often the result of many structural and chemical characteristics contributing synergistically at multiple length scales62,63. For example, the photonic nanostructures that produce vivid blue coloration in Morpho butterflies have inspired >50 articles on bioinspired materials15 and the optical properties of biophotonic crystals based on the Gyroid structure of some green butterflies is well understood (Fig. 2); yet we have limited experimental data on their biological function. Similarly, a twisted-ply (Bouligand) structure observed in insect cuticles has been found to improve the fracture toughness but its superiority compared with a simpler cross-ply structure – and hence its adaptive value – remains debatable64. In part, this is because structural characterizations are commonly based on specimens from museums, or purchased on the internet, with limited understanding of how these structures are used or their adaptive value in their natural environments. Determining function through behavioral and ecological investigation is often possible, but such investigations are invariably longer in duration than determining material structure. False assumptions about the biology of the model and discrepancy between biological function and the desired properties of the synthetic materials have been identified as two of the key obstacles to the successful development of bioinformed products45,65.

Linking structure to function and environment through multidisciplinary collaboration

To improve our ability to develop multifunctional bioinformed materials, there needs to be a concerted collaborative effort to link biological structures to the environments in which they occur, and ideally, to the multiple functions they serve45. As an example, such efforts have allowed us to explore the outstanding mechanical performance of highly mineralized biological materials such as bone and nacre in hydrated environments66, and the loss of this functionality upon desiccation67. Importantly, collaborative efforts to integrate materials science and biology provide reciprocal benefits68: materials scientists/engineers can greatly streamline the design process by understanding a biological material within its environmental context, and such collaborations can lead to “engineering-enabled biology” where a biological system or process can be examined from an engineering perspective to test novel functional hypotheses69.

We acknowledge the non-trivial barriers to such multidisciplinary collaborations. For example, the goals of biologists and materials engineers/designers seldom align, and the answers to questions posed by biologists are often not easily transferable to the problems engineers face69. Nevertheless, there are significant efforts to bridge the gap between biological and engineering approaches, including the communication and development of shared research objectives which inform the interests of both biologists and materials engineers/designers alike70. Although collaboration across fields can be challenging, it has clear benefits for innovation, and is increasingly becoming a strategic research priority.

Design and manufacture of bioinformed materials

Design approaches

Innovations are typically characterized as emanating from either technology push or market pull54,71. In the case of bioinformed materials, most efforts are technology pushed, meaning that the efforts focus on improving some new seemingly interesting technology and expecting to find a market for it once its usefulness is proven (Box 2). The market pull type technologies, on the other hand, build on a need identified in the market. This need triggers or guides technology development. Both are valid approaches but from the design point of view, a market need is essential for ultimate success72,73. One potential we identify here is the efficiency of natural systems optimized for performance in a specific environment, rather than a direct one-to-one mapping between function and form. In engineering this is called an integral system (as opposed to a modular system). These performance efficiencies are desired but they also complicate the design process due to the numerous interdependencies between the sub-systems74. There are systems engineering methods that engineers use to support this process75, however they are rarely applied to biological systems. In materials design, a common approach to achieve non-one-to-one mapping with function and material properties is to use composites. They generally outperform other materials due to their engineered properties, but often suffer from poor recyclability at the end of the material’s life76.

The challenges of scale and material composition

An important challenge for bioinformed materials design is the frequent mismatch between the scale of the biological model and the synthetic material (Fig. 4)37. The function of a material derives from its forms, processes, forces, and behaviour, which often change with physical scale. For instance, a microliter drop of water will bounce off a surface, whereas a basket-ball sized volume of water will splash because the surface tension acting on it is insufficient to hold the increased mass of liquid. Different forces dominate at different length scales, with molecular interactions at the nanoscale, interactions with light at the nanoscale and microscale, capillary/interfacial effects at the micrometer and millimeter scale, and gravity dominating at larger length scales. In other words, geometric similarity almost never corresponds to dynamic or functional similarity77. We must therefore ask: how does function change with physical scale? If we attempt to scale up a structure or material, does it lose the key characteristics? There are also hierarchical properties of scale, and emergent properties when shifting from one scale to another, making it frequently difficult to predict the effects of scaling up materials62. To address these many problems in scaling and material composition, we can observe how these problems are solved in natural models. For example, adhesive pad area appears to increase with body mass, although maintaining a pad size proportional to body size requires drastic morphological changes78. To compensate, some animals such as tree frogs appear to increase the efficiency of their adhesive pads with increasing body mass78, therefore such insights provide an important basis for designing adhesive attachment systems at larger size scales. These biological principles can then be represented as a digital model or virtual simulation to enable physical and mathematical analyses at scales of interest79.

Fig. 4: Different considerations of scale during the design and manufacture of a bioinformed material.
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a Different species can exhibit different solutions to a similar functional need. For example, adaptations for surface adhesion can be observed in small invertebrates such as beetles and spiders, as well as larger vertebrates such as geckos. Differences in individual adhesion strategies can reflect differences in scale as different forces dominate at each scale. b Biological materials are often complex and hierarchical and can comprise multiple adaptations at different scales. For example, not only are the microscopic setae on each toepad important for adhesion, but the muscles, tendons, and digit orientation have a significant effect on overall surface attachment96,97. c Biologically informed solutions can be applied at different scales depending on the desired performance of the material. It is important to evaluate how a shift in scale may change the effectiveness of a biological solution applied to materials. d The manufacture of a material can also present challenges depending on its scale; for example, not every nanoscale structure can be easily mass produced. Image of gecko foot is in the public domain from Wikipedia Commons by David Clements. Silhouette images from unsplash.com.

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Another major challenge is material composition. The extraordinary diversity of life’s designs is achieved using a few abundant organic and inorganic materials such as silks, chitin, keratin, cellulose, calcium carbonate and silica. The use of biopolymers such as chitosan and cellulose for materials innovation is gaining substantial momentum because they are (bio)degradable, among other advantages (Box 2)80,81,82; however, they are often less durable than synthetic materials. In general, a circular economy encourages minimal material use while also requiring materials to be as durable as possible due to the energy inputs into production and distribution. Further, materials should ultimately be reusable and recyclable, for which composite materials may be difficult to break down into constituents for reuse76,83. However, composites of biodegradable materials may offer new and so far, poorly explored opportunities for high performance materials (Box 2)24,27,84.

To some extent, considerations of scale and material composition can be addressed through careful material selection and performance evaluation against key criteria, including function and physical properties at different length scales. Increasingly, material selection criteria also include sustainability indicators such as carbon footprint, embodied energy (direct and indirect energy inputs from cradle-to-gate or cradle-to-grave), recycled content, material recyclability and other environmental indicators (e.g. biodegradability, water use, material longevity)85. Indeed, sustainability is a key focus of the materials selection framework developed by Ashby and colleagues86,87, with sustainability criteria incorporated into the associated material selection tool (Eco-Selector Tool in the Granta Ansys Materials Selector software88). The use of clearly defined material selection and performance evaluation criteria can help to refine the list of candidate materials appropriate for design and development of novel bioinformed materials.

Manufacture and cost

Many of the most promising functions of biological materials are achieved through elegant architectures at the nanometer and micron scale, and there are significant challenges around scaling up nanoscale structures to large surface areas or volumes22. Considerations include the expense of testing as well as cost of manufacture (current cost, as well as the likelihood that costs may come down), reliability (will the material have a long life?) and feasibility. Cost is a key consideration for all material production, but particularly for synthetic materials that replicate complex, composite or modular, and hierarchical features of biological materials because these features may increase the number of processing steps, the time taken to process, and so require more costly processing approaches.

Nevertheless, in some cases, certain nanoscale features can be replicated at scale relatively easily and cheaply. For example, self-cleaning surface coatings with superhydrophobic properties require the fabrication of micro- and nanoscale features that are robust over large surface areas, and these can be achieved with intrinsically scalable methods such as spraying or large-scale printing89. Many other features, however, would require a significant nanofabrication effort, even at a small scale. For example, the nanopattern of one layer of the multi-layered silica frustules of diatoms can be replicated using cost-effective replica molding, but manufacturing the multi-layered structure is pushing the current limits of nanofabrication, be it via top-down or bottom-up approaches90. Industry has cost-effectively harnessed these nanostructures in a very different way: mining diatom fossils (diatomaceous Earth) for a range of applications.

Synthetic materials rely on industrial manufacturing systems to produce objects at scale and with speed. Techniques most widely used include extruding, casting, rolling, and assembling. These allow for some variety, but not the kind of dynamic, fractal changeability that biological material systems exhibit. Additive manufacturing offers some potential to achieve more diverse structures, but to date it suffers from slower speeds compared with mass manufacturing methods, which results in more costly items91,92. Arguably, cost is one of the greatest obstacles for translating knowledge about biological materials into materials that can replace synthetics. While new manufacturing systems, like digital printing and robotics, have the capacity to integrate morphological variety, the system scale change required to replace existing systems is expensive and a carbon intensive process. Additionally, we note that all of the typical barriers to industry uptake of research apply to bioinformed materials, from regulatory requirements to lack of incentives to reduce energy consumption. Ultimately, scaling up requires integration of multiple disciplines from the earliest stages of the design process, including researchers, manufacturers, approval bodies, and end users.

Conclusions and guiding principles for future bioinformed innovation

Bioinformed design approaches hold enormous promise for innovation to meet the challenges of a circular economy and sustainable world. Perhaps unsurprisingly, the best design is one that resembles the process and outcome of biological evolution, insofar as the design process is adaptive and designs are refined to optimize multiple functions simultaneously (that is, designed in a holistic way). We have outlined key challenges in harnessing biological knowledge for bioinformed materials innovation and for the design, manufacture, and uptake of such materials. Addressing these challenges will require more effective multidisciplinary integration from the earliest stages of the design process, including researchers, product designers, manufacturers, approval bodies, and end users. Based on deliberations from a multidisciplinary workshop, we suggest guiding principles for future bioinformed innovation.

  1. 1.

    A bioinformed approach to materials innovation and sustainability extends beyond inspiration from single species to incorporate insights from higher levels of biological organization, such as ecosystems, and should inform all stages of materials production. Like biological systems, it is imperative to take a holistic view of the properties we desire in materials, over their full lifecycle, rather than narrowly optimizing for a single, specific function. Ultimately, materials must be designed for a circular economy and assessed against sustainability indicators. Bioinformed enhancements to improve both functionality and sustainability should be considered at multiple stages of the material lifecycle.

  2. 2.

    We suggest that biological information used for bioinformed design should be explicitly linked to the environmental context of the organism. We advocate high through-put characterization of material architectures and properties at different length scales, with information made publicly available and linked to environmental context through curated, annotated, and georeferenced databases. These repositories should be augmented by libraries of packages for analyzing and coalescing data.

  3. 3.

    We urge an approach to materials innovation that capitalizes on the defining feature of the natural world: diversity, produced via evolution by natural selection. This approach may entail examining material properties in multiple related species to understand how they vary in relation to the environment, given similar material, evolutionary and developmental constraints. Alternatively, it may entail examining functional solutions to similar problems in unrelated species to uncover general principles. Such a diversity-driven approach enables materials design to capitalize on multiple types of biological information, in multiple ways. We acknowledge that a diversity-driven approach is more difficult and may require development of biomaterials databases, approaches to processing large quantities of complex data such as machine learning, and world-wide collaborations (e.g., citizen science, crowd sources).

  4. 4.

    A bioinformed approach ultimately entails a shift away from one-to-one mapping between form and function or material property. This ideally needs to be achieved through material structure (e.g., hierarchical or layered), rather than through composition (composites), to maximize our ability to reuse and recycle materials. Innovation in structural properties is arguably where a bioinformed approach to materials design holds most promise.

  5. 5.

    The ability to manufacture bioinformed materials cost-effectively and at scale remain significant obstacles. These may be overcome with continued developments in nanofabrication and additive manufacturing techniques. Cost and manufacture should be considered from the earliest stages of bioinformed materials design, to gauge whether features can be replicated at scale using currently scalable techniques or require more complex, costly or novel manufacturing approaches.

  6. 6.

    Market need, in addition to the socio-cultural and economic context are essential factors to consider in the design of bioinformed sustainable materials. These factors ultimately determine the success or failure of materials at market and underscore the imperative for multidisciplinary integration in materials innovation.