Cooperative behavior of a sacrificial bond network and elastic framework in providing self-healing capacity in mussel byssal threads

Abstract

The dissipative and self-healing properties of mussel byssal threads are critical for their function as anchoring fibers in wave-battered habitats and central to their emergence as an exciting model system for bio-inspired polymers. Much is now understood about the structure-function relationships defining this remarkable proteinaceous bio-fiber; however, the molecular mechanisms underlying the distinctive tough, viscoelastic and self-healing behavior are still unclear. Here, we investigate elastic and dissipative contributions from the primary load-bearing proteins in the distal region of byssal threads (the preCols) using X-ray diffraction (XRD) combined with in situ tensile testing. Specifically, we identified cross β-sheet structure in the preCol flanking domains that functions as an elastic framework, providing hidden length. Dissipative behavior was associated with a strain-rate dependent phase transition of a sacrificial network stabilized by strong, reversible cross-links. Based on these findings, we posit a new model for byssal thread deformation and self-healing.

pH‐Responsive Self‐Organization of Metal‐Binding Protein Motifs from Biomolecular Junctions in Mussel Byssus

“…Rather, the HRD peptides formed dense amyloid-like phases under appropriate conditions of concentration and pH without metal ions present (Figure 9). [2,41] Notably, recent X-ray diffraction studies of native distal byssal threads have identified the presence of amyloid-like cross β-sheet structure; [14] however, it is unclear from the present investigation whether HRDs would still form amyloid phases within the thread. [2,41] Notably, recent X-ray diffraction studies of native distal byssal threads have identified the presence of amyloid-like cross β-sheet structure; [14] however, it is unclear from the present investigation whether HRDs would still form amyloid phases within the thread.…”

“…[11,12] The central collagen domain has a typical [Gly-X-Y] n motif, forming a triple helical structure of ≈150 nm in length, which determines the fibrous structure and high stiffness of threads. [6] Flanking both sides of the elongated collagen helix are large extensible domains, [11,12] which form highly folded β-sheet structure in preCol-D and -NG [13,14] and likely possess an intrinsically disordered structure reminiscent of elastin in preCol-P. [12] At the N-and C-terminal ends of all preCols are the histidine-rich domains (HRDs) ( Figure 1C), [11,12,15,16] which are the least understood of all the preCol domains from a structural as well as functional perspective and which provide the main focus of the current study. Mounting evidence supports a critical role of the HRDs from preCol-D and -NG (≈20 mol% histidine) in regulating the mechanical response of the distal region of byssal threads, which is mediated through specific interactions of HRD histidine residues with transition metal ions (e.g., Zn, Cu, Ni) to create a mechanically functional network of intermolecular metal coordination cross-links.…”

Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication

“…The byssus core is an energy damping fibrous biopolymer comprised of a semi-crystalline array of collagenous proteins known as preCols (refs 9, 10). The core possesses an initial stiffness comparable to vertebrate tendon (nearly 900 MPa in some species)11; however, due to distinctive non-collagenous preCol domains, it is far more tough and extensible, and most notably, exhibits intrinsic self-healing capacity during cyclic loading1213. The cuticle, which surrounds the stretchy core, is thought to play a protective role against abrasion due to its unusual combination of high hardness (H=100 MPa for Mytilus galloprovincialis similar to an engineering epoxy) and high extensibility ( ɛ ult =70–100%)14.…”

Mussel Byssus Structure‐Function and Fabrication as Inspiration for Biotechnological Production of Advanced Materials

“…The plaque is a versatile underwater adhesive glue that serves as the interface between the byssal thread and the surface . The core of the thread is a fibrous bio‐polymer anchored into the plaque that provides the energy‐damping function . The cuticle is a thin sheath surrounding the core and plaque proposed to function as a protective coating .…”

“…The fibrous core of a byssal thread is believed to primarily determine its tensile mechanical properties . Threads have two distinct regions known as the distal and proximal thread, which are adjacent to the surface and mussel, respectively.…”