Alpha-helical protein domains unify strength and robustness through hierarchicalnanostructures

Abstract

Hierarchical nanostructures, ranging through atomistic, molecular and macroscopic scales,represent universal features of biological protein materials. Here we show for the case ofalpha-helical (AH) protein domains that this use of molecular hierarchies within thestructural arrangement leads to an extended physical dimension in the material designspace that resolves the conflict between disparate material properties such as strength androbustness, a limitation faced by many synthetic materials. An optimal combination ofredundancies at different hierarchical levels enables superior mechanical performancewithout additional material use. Our analysis is facilitated by the application of aHierarchical Bell model (HBM), which explicitly considers the hierarchical architecture ofH-bonds within the protein structure, providing a structure–property relationshipof strength properties of AH protein nanostructures. The HBM is validated bylarge-scale molecular dynamics simulations of several model protein structures.Our findings may enable the development of self-assembled de novo bioinspirednanomaterials based on peptide and protein building blocks, and could help inelucidating the mechanistic role of AHs in cell signaling and mechanotransduction.