Unraveling capillary interaction and viscoelastic response in atomic force microscopy of hydrated collagen fibrils

Abstract

The mechanical properties of collagen fibrils depend on the amount and the distribution of water molecules within the fibrils. Here, we use atomic force microscopy (AFM) to study the effect of hydration on the viscoelastic properties of reconstituted type I collagen fibrils in air with controlled relative humidity. With the same AFM tip, we investigate the same area of a collagen fibril with two different force spectroscopy methods: force-distance (FD) and amplitude-phase-distance (APD) measurements. This allows us to separate the contributions of the fibril's viscoelastic response and the capillary force to the tip-sample interaction. A water bridge forms between the tip apex and the surface, causing an attractive capillary force, which is the main contribution to the energy dissipated from the tip to the specimen in dynamic AFM. The force hysteresis in the FD measurements and the tip indentation of only 2 nm in the APD measurements show that the hydrated collagen fibril is a viscoelastic solid. The mechanical properties of the gap regions and the overlap regions in the fibril's D-band pattern differ only in the top 2 nm but not in the fibril's bulk. We attribute this to the reduced number of intermolecular crosslinks in the reconstituted collagen fibril. The presented methodology allows the mechanical surface properties of hydrated collagenous tissues and biomaterials to be studied with unprecedented detail on the nanometer scale.

Structure and Nanomechanics of Dry and Hydrated Intermediate Filament Films and Fibers Produced from Hagfish Slime Fibers

“…Therefore, a behavior similar to tough hydrogels 78 as well as viscoelasticity 79,80 were observed. Viscoelasticity is well-known for IFs 38,77,81 and indentation curves showing a similar recoverable hysteresis were observed for hydrated collagen fibrils 82 and stratum corneum 83 , cells 84 , as well as polyacrylamide, PVA hydrogels [84][85][86] , and PDMS 87,88 . In order to assess the viscoelastic behavior of the hydrated IF films, two different approaches were used.…”

Nanomechanical mapping of soft materials with the atomic force microscope: methods, theory and applications

“…318,319 The hydration of biopolymers under different conditions was followed by recording phase shift-distance curves. 320,321 Several viscoelastic processes on polymer blends and polymer nanocomposites have been studied by AFM phase contrast images. 322,323 The sensitivity of the phase shift signal has enabled to detect interfacial fluctuations on PS-b-PMMA, 324 to perform in situ studies of crystallization of polymers as a function of the temperature 325 or to image in realtime selfassembly processes.…”

Fast, quantitative and high resolution mapping of viscoelastic properties with bimodal AFM

“…The understanding, characterization and mapping of the viscoelastic properties of soft matter at the nanoscale level is an active area of research in polymer science, nanolithography, mechanobiology and force microscopy. [1][2][3][4][5][6][7][8][9][10][11][12] The development of novel nanolithographies demands a fast and high resolution characterization of the viscoelastic properties of polymer resists. 12,13 In mechanobiology, there is some evidence that supports the influence of the cell's viscoelastic processes in its physiology.…”