Nano-Mechanical and -Electromechanical Heterogeneity in Single Collagen Fibrils

Abstract

Type I collagen, as the most abundant protein in mammals, is the main organic component of bone, tendon, dentine, and cornea. Functioning in such diverse tissues shows the multifunctional capability of collagen fibrils. The gap and overlap regions in axial direction of a fibril with a characteristic period of ∼67 nm is believed to be an important factor in microstructure of the fibrils enabling its multifunctionality. For example, in bone mineral nano-crystals are deposited specifically in the gap region. In this study, we focus on studying mechanical and electromechanical properties at different scale levels, ranging from subfibrillar microstructure of single collagen fibrils ∼100 nm in diameter up to bone samples.In terms of mechanical (elastic and viscoelastic) properties, implementing near-surface static and dynamic nanoindentation technique with AFM, we show that the gap and overlap regions in single collagen fibril have significantly different elastic and energy dissipation properties, correlating the significantly different molecular structures in these two regions. We further show that such subfibrillar heterogeneity holds in collagen fibrils inside bone and might be related to the excellent energy dissipation performance of bone.It is known that bone and tendon are piezoelectric, and it is believed that the piezoelectric charges produced under mechanical deformation in these tissues have a potential role in mechanoelectric transduction leading to their growth and remodeling. With high resolution PFM we probe piezoelectric properties in bone and show that single collagen fibrils are responsible for piezoelectric behavior of bone and behave predominantly as shear piezoelectric materials. Furthermore, we show that there is an intrinsic electromechanical heterogeneity in axial direction of individual fibrils that holds even for the collagen fibrils embedded in bone matrix. Such heterogeneity may have implications in regulating the ionic environment in bone responsible for bone remodeling.