Structural architectures with toughening mechanisms in Nature: A review of the materials science of Type-I collagenous materials

The structural constituents of tissues in organisms are composed primarily of minerals and proteins. Collagen is the most common protein used to construct such natural materials in vertebrates; among these structures, a wide variety of hierarchical architectures with structural and property gradients have evolved to induce desired combinations of stiffness, strength, ductility and toughness for a diverse range of mechanical functionalities. The soft collagen provides biological materials the ability to resist tensile tractions and to dissipate energy under mechanical deformation. Here we seek to understand the structure, deformation and toughening mechanisms of collagenous materials from the perspective of the hierarchical assembly of individual collagen molecules, fibrils, fibers, as well as the other nature-designed hierarchical structural elements. This review summarizes the structural designs of collagenous materials focusing on Type-I collagen, the most abundant extracellular protein that forms linear arrays, as well as examining its deformation and toughening mechanisms by illustrating how nature uses hierarchical structures and gradients, at nano-, micro- to macro-levels, to confer different functions to its organisms. The organization of collagen is discussed for different structures in order to illustrate the broad range of its functional and mechanical properties: specifically, skin, arteries, eye cornea, fish scales, bone, ligaments and tendons. We conclude by highlighting important developments in tissue engineering where synthetic and natural collagen has been incorporated into the architecture of the body. We trust that such insight may provide guidance for the design of the next-generation of synthetic structural materials with unprecedented functionality.