Stress controls the mechanics of collagen networks

Significance We report nonlinear rheology experiments on collagen type I networks, which demonstrate a surprising concentration independence of the network stiffness in the nonlinear elastic regime. We develop a model that can account for this, as well as the classical observations of an approximate exponential stress–strain relationship in collagenous tissues, for which a microscopic model has been lacking. Our model also demonstrates the importance of normal stresses in controlling the nonlinear mechanics of fiber networks. Collagen is the main structural and load-bearing element of various connective tissues, where it forms the extracellular matrix that supports cells. It has long been known that collagenous tissues exhibit a highly nonlinear stress–strain relationship, although the origins of this nonlinearity remain unknown. Here, we show that the nonlinear stiffening of reconstituted type I collagen networks is controlled by the applied stress and that the network stiffness becomes surprisingly insensitive to network concentration. We demonstrate how a simple model for networks of elastic fibers can quantitatively account for the mechanics of reconstituted collagen networks. Our model points to the important role of normal stresses in determining the nonlinear shear elastic response, which can explain the approximate exponential relationship between stress and strain reported for collagenous tissues. This further suggests principles for the design of synthetic fiber networks with collagen-like properties, as well as a mechanism for the control of the mechanics of such networks.