Structural hierarchy confers error tolerance in biological tissues

Disordered networks of semiflexible filaments are common support structures in biology. Familiar examples include fibrous matrices in blood clots, bacterial biofilms, and essential components of cells and tissues of plants, animals, and fungi. Despite the ubiquity of these networks in biomaterials, we have only a limited understanding of the relationship between their structural features and highly strain-sensitive mechanical properties. In this work, we perform simulations o...

We propose a class of microstructurally informed models for the linear elastic mechanical behavior of cross-linked polymer networks such as the actin cytoskeleton. Salient features of the models include the possibility to represent anisotropic mechanical behavior resulting from anisotropic filament distributions, and a power-law scaling of the mechanical properties with the filament density. Mechanical models within the class are parameterized by seven different constants. We...

Hierarchical structures with constituents over multiple length scales are found in various natural materials like bones, shells, spider silk and others, all of which display enhanced quasi-static mechanical properties, such as high specific strength, stiffness and toughness. At the same time, the role of hierarchy on the dynamic behaviour of metamaterials remains largely unexplored. This study assesses the effect of bio-inspired hierarchical organization as well as of viscoel...

We present a theory for the toughness, damage tolerance, and tensile strength of a class of hierarchical, fractal, metamaterials. We show that the even though the absolute toughness and damage tolerance decrease with increasing number of hierarchical scales, the specific toughness (toughness per-unit density) grows with increasing number of hierarchical scales in the material, while the specific tensile strength and damage tolerance remain constant.

Living matter moves, deforms, and organizes itself. In cells this is made possible by networks of polymer filaments and crosslinking molecules that connect filaments to each other and that act as motors to do mechanical work on the network. For the case of highly cross-linked filament networks, we discuss how the material properties of assemblies emerge from the forces exerted by microscopic agents. First, we introduce a phenomenological model that characterizes the forces th...

Computer simulations can aid in understanding how collective materials properties emerge from interactions between simple constituents. Here, we introduce a coarse-grained model that enables simulation of networks of actin filaments, myosin motors, and crosslinking proteins at biologically relevant time and length scales. We demonstrate that the model qualitatively and quantitatively captures a suite of trends observed experimentally, including the statistics of filament fluc...

Shape-morphing networks of mesoscale filaments are a common hierarchical feature in biology and hold significant potential for a range of technological applications, from micro-muscles to shape-morphing optical devices. Here, we demonstrate both experimentally and computationally that the shape-morphing of highly-ordered 2D networks constructed of thermoresponsive mesoscale polymeric fibers strongly depends on the physical attributes of the single fiber, in particular on its ...

Fibrous networks are ideal functional materials since they provide mechanical rigidity at low weight. Such structures are omnipresent in natural biomaterials from cells to tissues, as well as in man-made materials from polymeric composites to paper and textiles. Here, we demonstrate that fibrous networks of the blood clotting protein fibrin undergo a strong and irreversible increase in their mechanical rigidity in response to compression. This rigidification can be precisely ...

Strain stiffening of protein networks is explored by means of a finite strain analysis of a two-dimensional network model of cross-linked semiflexible filaments. The results show that stiffening is caused by non-affine network rearrangements that govern a transition from a bending dominated response at small strains to a stretching dominated response at large strains. Thermally-induced filament undulations only have a minor effect; they merely postpone the transition.

Nature provides examples of self-assemble lightweight disordered network structures with remarkable mechanical properties which are desirable for many applications purposes but challenging to reproduce artificially. Previous experimental and computational studies investigated the mechanical responses of random network structures focusing on topological and geometrical aspects in terms of variable connectivity or probability to place beam elements. However for practical purpos...