Why and How to Investigate Biological Materials Processing: A Cross-Disciplinary Approach for Inspiring Sustainable Materials Fabrication

Abstract

Enhancing the performance and sustainability of materials is a major challenge facing humanity. With nearly 400 million tons of plastics manufactured per year and plastic waste accumulation of 12 billion tons expected by 2050, the production and buildup of anthropogenic petroleum-based waste is a major threat to our global ecosystem. This impending environmental catastrophe demands alternative sustainable and circular routes for material production. Additionally, there is a need for new polymeric materials that possess properties not currently found in synthetic materials for various applications in biomedical engineering, soft robotics, flexible electronics, and more. Nature offers inspiration for solving both of these environmentally, economically, and socially impactful global issues. Indeed, living organisms, such as spiders and mussels, rapidly fabricate polymeric biological materials from biomolecular building blocks (e.g., proteins) under green, environmentally benign processing conditions. These materials exhibit properties that surpass many synthetic plastics (e.g., high toughness, self-healing, “smart” adaptability, underwater adhesion), providing a blueprint for how humans can develop sustainable fabrication practices for producing next-generation materials. There is now a solid understanding of the structure–function relationships defining the performance of many biological materials, with control of structural hierarchy from nanoscale to centimeter scale emerging as a common design feature. Yet, it has been extremely challenging to replicate this hierarchical structure and, thus, the relevant properties in synthetic materials. This is largely due to a poor understanding of how these materials are fabricated by living organisms. Indeed, elucidation of the physicochemical principles underlying the fabrication of these and similar materials is significantly hampered due to experimental challenges in following these dynamic processes at the relevant spatiotemporal scales. Here, I outline a cross-disciplinary experimental approach spanning organismal biology, molecular biology, biochemistry, physical chemistry, and materials science for extracting design principles from biofabrication processes. As a model system, I focus on the fabrication of the mussel byssus–a biopolymeric fibrous holdfast with outstanding properties (underwater adhesion, high toughness, self-healing capacity) that is an established archetype for sustainable bioinspired fibers, glues, composites, and coatings. Careful analysis combining traditional histology and biochemical approaches with advanced spectroscopic imaging (e.g, confocal Raman spectroscopy, FTIR spectroscopy, and micro X-ray fluorescence), tomographic approaches (e.g., micro-CT), and advanced electron microscopy (e.g., focused ion beam scanning electron microscopy (FIB-SEM)) have yielded deep insights into the byssus assembly process, highlighting the key role of fluid protein condensates (liquid crystals and coacervates), microfluidic-like mixing, and protein–metal coordination bonds, as well as various physicochemical triggers (e.g., pH, redox, mechanical shear) that promote the self-organization and cross-linking of stimuli-responsive protein building blocks. Extracted concepts are already being applied for enhancing the sustainable fabrication of bioinspired materials for technical and biomedical applications.