Protein-based biogenic materials provide important inspiration for the development of high-performance polymers. The fibrous mussel byssus, for instance, exhibits exceptional wet adhesion, abrasion ...resistance, toughness and self-healing capacity-properties that arise from an intricate hierarchical organization formed in minutes from a fluid secretion of over 10 different protein precursors. However, a poor understanding of this dynamic biofabrication process has hindered effective translation of byssus design principles into synthetic materials. Here, we explore mussel byssus assembly in Mytilus edulis using a synergistic combination of histological staining and confocal Raman microspectroscopy, enabling in situ tracking of specific proteins during induced thread formation from soluble precursors to solid fibres. Our findings reveal critical insights into this complex biological manufacturing process, showing that protein precursors spontaneously self-assemble into complex architectures, while maturation proceeds in subsequent regulated steps. Beyond their biological importance, these findings may guide development of advanced materials with biomedical and industrial relevance.
Protein‐metal interactions—traditionally regarded for roles in metabolic processes—are now known to enhance the performance of certain biogenic materials, influencing properties such as hardness, ...toughness, adhesion, and self‐healing. Design principles elucidated through thorough study of such materials are yielding vital insights for the design of biomimetic metallopolymers with industrial and biomedical applications. Recent advances in the understanding of the biological structure–function relationships are highlighted here with a specific focus on materials such as arthropod biting parts, mussel byssal threads, and sandcastle worm cement.
Protein–metal interactions were traditionally regarded for their role in metabolic processes. Nowadays, they are also known to enhance the performance of certain biogenic materials, influencing properties such as hardness, toughness, adhesion, and self‐healing. In this Review, recent advances in the understanding of the biological structure–function relationships are highlighted.
Natural load-bearing protein materials Harrington, Matthew J.; Fratzl, Peter
Progress in materials science,
July 2021, 2021-07-00, 20210701, Letnik:
120
Journal Article
Recenzirano
Biological tissues in animals generally consist an extracellular matrix often with cells embedded in it. These materials are primarily comprised of different protein building blocks, as well as ...polysaccharide and mineral components in certain cases. Prominent examples include tendon, skin and bone. In contrast, other organisms fabricate protein-based materials that function extracorporeally – that is, outside the body and without embedded living cells. Typical examples include spider and insect silk or the byssus filaments by which mussels attach to rocks. Regardless of whether these materials function inside or outside the body and whether or not they contain living cells, natural protein-based materials perform essential life functions that are very often highly dependent on their load-bearing mechanical properties. In the current review, we explore the relationship between specific features of these protein building blocks (e.g. their sequence, conformation, cross-linking and hierarchical structure) and the higher-level mechanical function of the materials that they comprise. The extracted structure–property relationships have crucial importance for understanding the biological function of these materials, but also have implications for bio-inspired design of new polymers and composites, as well as relevance for ongoing efforts to bioengineer artificial tissues.
The extensible byssal threads of marine mussels are shielded from abrasion in wave-swept habitats by an outer cuticle that is largely proteinaceous and approximately fivefold harder than the thread ...core. Threads from several species exhibit granular cuticles containing a protein that is rich in the catecholic amino acid 3,4-dihydroxyphenylalanine (dopa) as well as inorganic ions, notably Fe³⁺. Granular cuticles exhibit a remarkable combination of high hardness and high extensibility. We explored byssus cuticle chemistry by means of in situ resonance Raman spectroscopy and demonstrated that the cuticle is a polymeric scaffold stabilized by catecholato-iron chelate complexes having an unusual clustered distribution. Consistent with byssal cuticle chemistry and mechanics, we present a model in which dense cross-linking in the granules provides hardness, whereas the less cross-linked matrix provides extensibility.
There is an urgent need to improve the sustainability of the materials we produce and use. Here, we explore what humans can learn from nature about how to sustainably fabricate polymeric fibers with ...excellent material properties by reviewing the physical and chemical aspects of materials processing distilled from diverse model systems, including spider silk, mussel byssus, velvet worm slime, hagfish slime, and mistletoe viscin. We identify common and divergent strategies, highlighting the potential for bioinspired design and technology transfer. Despite the diversity of the biopolymeric fibers surveyed, we identify several common strategies across multiple systems, including: (1) use of stimuli-responsive biomolecular building blocks, (2) use of concentrated fluid precursor phases (e.g., coacervates and liquid crystals) stored under controlled chemical conditions, and (3) use of chemical (pH, salt concentration, redox chemistry) and physical (mechanical shear, extensional flow) stimuli to trigger the transition from fluid precursor to solid material. Importantly, because these materials largely form and function outside of the body of the organisms, these principles can more easily be transferred for bioinspired design in synthetic systems. We end the review by discussing ongoing efforts and challenges to mimic biological model systems, with a particular focus on artificial spider silks and mussel-inspired materials.
Growing evidence supports a critical role of metal-ligand coordination in many attributes of biological materials including adhesion, self-assembly, toughness, and hardness without mineralization ...Rubin DJ, Miserez A, Waite JH (2010) Advances in Insect Physiology: Insect Integument and Color, eds Jérôme C, Stephen JS (Academic Press, London), pp 75-133. Coordination between Fe and catechol ligands has recently been correlated to the hardness and high extensibility of the cuticle of mussel byssal threads and proposed to endow self-healing properties Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P (2010) Science 328:216-220. Inspired by the pH jump experienced by proteins during maturation of a mussel byssus secretion, we have developed a simple method to control catechol-Fe³⁺ interpolymer cross-linking via pH. The resonance Raman signature of catechol-Fe³⁺ cross-linked polymer gels at high pH was similar to that from native mussel thread cuticle and the gels displayed elastic moduli (G') that approach covalently cross-linked gels as well as self-healing properties.
To anchor in seashore habitats, mussels fabricate adhesive byssus fibers that are mechanically reinforced by protein-metal coordination mediated by 3,4-dihydroxyphenylalanine (DOPA). The mechanism by ...which metal ions are integrated during byssus formation remains unknown. In this study, we investigated the byssus formation process in the blue mussel,
, combining traditional and advanced methods to identify how and when metals are incorporated. Mussels store iron and vanadium ions in intracellular metal storage particles (MSPs) complexed with previously unknown catechol-based biomolecules. During adhesive formation, stockpiled secretory vesicles containing concentrated fluid proteins are mixed with MSPs within a microfluidic-like network of interconnected channels where they coalesce, forming protein-metal bonds within the nascent byssus. These findings advance our understanding of metal use in biological materials with implications for next-generation metallopolymers and adhesives.
Biotechnology offers an exciting avenue toward the sustainable production of high performance proteinaceous polymeric materials. In particular, the mussel byssus—a high performance adhesive bio‐fiber ...used by mussels to cling on hard surfaces—has become a veritable archetype for bio‐inspired self‐healing fibers, tough coatings, and versatile wet adhesives. However, successful translation of mussel‐inspired design principles into man‐made materials hinges upon elucidating structure‐function relationships and biological fabrication processes. This review provides a detailed survey of the state‐of‐the‐art understanding of the biochemical structure‐function relationships defining byssus performance with a particular focus on structural hierarchy and metal coordination‐based cross‐linking. The efforts to mimic the byssus in man‐made materials are then discussed. While there has been a strong push to mimic the byssus via synthetic chemistry taking a reductionist approach, herein the focus is specifically on recent progress of biotechnology‐based strategies that more closely approximate the biochemical complexity of the natural material. As an outlook, an overview of recent research toward understanding the natural byssus assembly process is provided, as processing remains a critical factor in achieving native‐like properties.
Protein‐based materials produced by biological organisms from protein building blocks are important archetypes for future development of sustainable, advanced materials, and biotechnology offers great potential as a translational technology. Herein are reviewed relevant extracted design principles from the structure‐function relationships and fabrication of the mussel byssus—a collection tough and self‐healing adhesive bio‐fiber produced by mussels. Recent progress in biotechnological production of mussel‐inspired materials is highlighted. This article is part of the an AFOB (Asian Federation of Biotechnology) Special Issue. To learn more about the AFOB visit www.afob.org.
This article is part of an AFOB (Asian Federation of Biotechnology) Special issue. To learn more about the AFOB visit www.afob.org.
Complex hierarchical structure governs emergent properties in biopolymeric materials; yet, the material processing involved remains poorly understood. Here, we investigated the multi-scale structure ...and composition of the mussel byssus cuticle before, during and after formation to gain insight into the processing of this hard, yet extensible metal cross-linked protein composite. Our findings reveal that the granular substructure crucial to the cuticle's function as a wear-resistant coating of an extensible polymer fiber is pre-organized in condensed liquid phase secretory vesicles. These are phase-separated into DOPA-rich proto-granules enveloped in a sulfur-rich proto-matrix which fuses during secretion, forming the sub-structure of the cuticle. Metal ions are added subsequently in a site-specific way, with iron contained in the sulfur-rich matrix and vanadium coordinated by DOPA-catechol in the granule. We posit that this hierarchical structure self-organizes via phase separation of specific amphiphilic proteins within secretory vesicles, resulting in a meso-scale structuring that governs cuticle function.
Bottom-up control over structural hierarchy from the nanoscale through the macroscale is a critical aspect of biological materials fabrication and function, which can inspire production of advanced ...materials. Mussel byssal threads are a prime example of protein-based biofibers in which hierarchical organization of protein building blocks coupled via metal complexation leads to notable mechanical behaviors, such as high toughness and self-healing. Using a natural amino acid sequence from byssal thread proteins, which functions as a pH-triggered self-assembly point, we created free-standing peptide films with complex hierarchical organization across multiple length scales that can be controlled by inclusion of metal ions (Zn2+ and Cu2+) during the assembly process. Additionally, analysis of film mechanical performance indicates that metal coordination bestows up to an order of magnitude increase in material stiffness, providing a paradigm for creating tunable polymeric materials with multiscale organizational structure.
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