Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils

Abstract

Spider silk is one of the strongest, most extensible and toughest biological materials known, exceeding the properties of many engineered materials including steel. Silks feature a hierarchical architecture where highly organized, densely H-bonded beta-sheet nanocrystals are arranged within a semi-amorphous protein matrix consisting of 31-helices and beta-turn protein structures. By using a bottom-up molecular-based mesoscale model that bridges the scales from Angstroms to hundreds of nanometers, here we show that the specific combination of a crystalline phase and a semi-amorphous matrix is crucial for the unique properties of silks. Specifically, our results reveal that the superior mechanical properties of spider silk can be explained solely by structural effects, where the geometric confinement of beta-sheet nanocrystals combined with highly extensible semi-amorphous domains with a large hidden length is the key to reach great strength and great toughness, despite the dominance of mechanically inferior chemical interactions such as H-bonding. Our model directly shows that semi-amorphous regions unravel first when silk is being stretched, leading to the large extensibility of silk. Conversely, the large-deformation mechanical properties and ultimate tensile strength of silk is controlled by the strength of beta-sheet nanocrystals, which is directly related to their size, where small beta-sheet nanocrystals are crucial to reach outstanding levels of strength and toughness. Our model agrees well with observations in recent experiments, where it was shown that a significant change in the strength and toughness can be achieved solely by tuning the size of beta-sheet nanocrystals. Our findings unveil the material design strategy that enables silks to achieve superior material performance despite simple and inferior constituents, resulting in a new paradigm in materials design where enhanced functionality is not achieved using complex building blocks, but rather through the utilization of simple repetitive constitutive elements arranged in hierarchical structures.

Relationship between structural composition and material properties of polymorphic hIAPP fibrils

“…These results can be compared with our previous results, which applied constant force and velocity according to different bending directions [30,31]. Furthermore, the results can also be compared with spider silk, which is mainly composed of rich β strands with various crystal areas [39,40]. Although different loading conditions have been applied in this study to compare our results to previous studies, we observed the similar fracture toughness of polymorphic hIAPP fibrils.…”

Diversity of Molecular Transformations Involved in the Formation of Spider Silks

“…The length of the polyalanine motifs is not only optimized with respect to the secondary structure that they adopt but also optimized with respect to the size of the β-sheet nanocrystals of the fiber, since the mechanical properties of the Ma thread decrease as the crystal size increases. 51 The spacer region of MiSp1 probably contains some α-helix segments. Finally, Cyl and Ac proteins are predicted to adopt significant amounts of α-helices.…”

Ballistic impact to access the high-rate behaviour of individual silk fibres

“…Such an interpretation is also supported by more recent molecular dynamics simulations on b-sheet structures in silk and their contribution towards mechanical properties (Nova et al, 2010).…”