Structural heterogeneity in silk fibers and its effects on failure mechanics and supercontraction

Abstract

Spider dragline silk is a protein material that has evolved over millions of years to become one of the strongest and toughest natural fibers known. Silk features a heterogeneous structure that comprises [beta]-sheet crystals embedded in an amorphous matrix. However, it is not fully understood how the heterogeneity of silk affects its mechanical properties. First, the origin of the nanoscale heterogeneity during the Nephila Clavipes dragline silk assembly is investigated. Using molecular dynamics simulations, a shear flow at natural pulling speeds is modelled and the secondary structure transitions as well as shear stresses in the silk protein chains are determined. It is shown that under shear stresses beyond the elastic regime, silk undergoes an [alpha] -- [beta] transition in the spinning duct. The stability of the assembled [beta]-sheet structure seems to arise from a close proximity of the [alpha]-helices in the silk solution. The smallest molecule size that might give rise to a silk-like structure is determined to comprise four to six repeats of the silk sequence. Establishing the molecular details of the assembly can guide the design of microfluidic devices and the synthesis of bioinspired protein materials. Second, it is shown how the heterogeneity of silk fibers, specifically its crystalline phase, relates to its fracture mechanical properties: strength and toughness. Analytical fracture mechanical arguments are presented to illustrate the relation between fracture strength and heterogeneity in silk and other biopolymers. Nanoconfinement and flaw tolerance are presented as natural strategies to increase the mechanical performance of the entire material system. It is shown that the consideration of interatomic interactions alone cannot explain the fracture strength observed in biological fibers. Instead, structures at multiple length-scales must be considered to explain the remarkable mechanical performance and resilience of silk. Third, the interaction of water with silk's heterogeneous nanostructure is investigated. At high humidity, some spider dragline silks will shrink up to 50%, a phenomenon known as supercontraction. The molecular origin of dragline silk supercontraction is explored using a full-atomistic model and molecular dynamics supported by in situ Raman spectroscopy and mechanical testing performed at the Max Planck Institute in Potsdam, Germany. Tyrosine and Arginine are identified as the key residues in the Nephila Clavipes silk sequence that control supercontraction. A genetic engineering strategy to alter silk's behavior to industrial requirements is proposed, where sequence mutations reduce or even reverse the supercontraction mechanism.