Rough Fibrils Provide a Toughening Mechanism in Biological Fibers

Abstract

Spider silk is a fascinating\ud natural composite material. Its combination\ud of strength and toughness is unrivalled in\ud nature, and as a result, it has gained considerable\ud interest from the medical, physics,\ud and materials communities. Most of this\ud attention has focused on the one to tens of\ud nanometer scale: predominantly the primary\ud (peptide sequences) and secondary (β sheets,\ud helices, and amorphous domains) structure, with some insights into tertiary structure (the\ud arrangement of these secondary structures) to describe the origins of the mechanical and\ud biological performance. Starting with spider silk, and relating our findings to collagen fibrils,\ud we describe toughening mechanisms at the hundreds of nanometer scale, namely, the fibril\ud morphology and its consequences for mechanical behavior and the dissipation of energy.\ud Under normal conditions, this morphology creates a nonslip fibril kinematics, restricting\ud shearing between fibrils, yet allowing controlled local slipping under high shear stress,\ud dissipating energy without bulk fracturing. This mechanism provides a relatively simple target\ud for biomimicry and, thus, can potentially be used to increase fracture resistance in synthetic\ud materials

Increasing silk fibre strength through heterogeneity of bundled fibrils

“…Such behaviour was only achieved provided that the fibrils were confined to dimensions below a critical length scale on the order of approximately 20-80 nm [37]. Experimental results indicate silk fibrils on the order of 20-200 nm in diameter [18,[38][39][40][41], suggesting a length scale in accordance with the benefits of such nanoconfinement. Moreover, another study [42]-motivated by continuum fracture mechanics criteria-indicated that silk toughness does not depend directly on nanostructure, but rather cohesive energy density (in collusion with a modulus contribution), and the fracture mechanics characteristics depends on micrometrescale dimensional features and attributable to its fineness.…”

“…That being said, few studies have explicitly considered the contribution of interfibril interactions to the response of a thread. Recent atomic force microscopy (AFM) imaging has indicated that these fibrils are not homogeneous along the axis-they are characterized by globular protrusions at regular intervals ( figure 2a,b), increasing the fibril diameter over 50 per cent [41]. It has been proposed that these globules effectively form shear keys [41].…”

“…Recent atomic force microscopy (AFM) imaging has indicated that these fibrils are not homogeneous along the axis-they are characterized by globular protrusions at regular intervals ( figure 2a,b), increasing the fibril diameter over 50 per cent [41]. It has been proposed that these globules effectively form shear keys [41]. The same investigation implemented a two-dimensional finite-element model to focus on the fibril-fibril interface and the effect of heterogeneous globules/protrusions [41].…”

“…It has been proposed that these globules effectively form shear keys [41]. The same investigation implemented a two-dimensional finite-element model to focus on the fibril-fibril interface and the effect of heterogeneous globules/protrusions [41]. Indeed, it was shown that the globular structures resulted in non-slip kinematics, restricted fibril shearing, controlled slippage, stress transfer as well as energy dissipation [41].…”

“…The same investigation implemented a two-dimensional finite-element model to focus on the fibril-fibril interface and the effect of heterogeneous globules/protrusions [41]. Indeed, it was shown that the globular structures resulted in non-slip kinematics, restricted fibril shearing, controlled slippage, stress transfer as well as energy dissipation [41]. An analogy was made to bone and nacre, wherein the roughness of interfaces [49] and layer bridging [50,51] results in strong and tough materials [52,53].…”