Multimodal X-ray imaging reveals hierarchical fibre mechanics

Abstract

Abstract Fibrous materials, ranging from connective tissues 1–4 to engineered composites 5–8 , are vital to many biological and man-made systems, optimized to withstand complex in operando or in vivo loading. The load-bearing capacity of intervertebral discs (IVDs) of the spine depends on a hierarchical extracellular matrix, where plywood-like lamellae of collagen fibres in the annulus fibrosus contain nanometre-scale fibrils built from staggered triple-helical monomers 4,9,10 . How intact IVDs couple fibril-scale mechanics to fibre-scale organization under load remains unresolved. Here we introduce TomoSAXS, a full-field 3D small-angle X-ray scattering tomography that maps fibril-to-fibre mechanics across an intact tissue. We show that intrafibrillar molecular pre-strain (D-period stagger) is lamellar textured and tightly correlated with microscale fibre strain. Pre-strain is inversely related to fibril strain and its variability, consistent with load-sharing through molecular unwinding. Radial strain bridges and high-curvature zones at the annulus fibrosus–nucleus pulposus interfaces emerge as critical regulators of local mechanics. These findings reveal concerted fibril–fibre interactions that sustain mechanical equilibrium in the IVD, preserving elasticity and shape. More broadly, TomoSAXS establishes a platform to visualize nanoscale-to-microscale matrix mechanics across biological and synthetic fibrous materials, with applications in ageing and disease, therapeutic evaluation and the design of bio-based and bio-inspired materials.