Dynamic and Programmable Cellular-Scale Granules Enable Tissue-like Materials

Living tissues are an integrated, multiscale architecture consisting of dense cellular ensembles and extracellular matrices (ECMs). The cells and ECMs cooperate to enable specialized mechanical properties and dynamic responsiveness. However, the mechanical properties of living tissues are difficult to replicate. A particular challenge is identification of a cell-like synthetic component, which is tightly integrated with its matrix and also responsive to external stimuli. Here, we demonstrate that cellular-scale hydrated starch granules, an underexplored component in materials science, can turn conventional hydrogels into tissue-like materials when composites are formed. By using several synchrotron-based X-ray techniques, we reveal the mechanically induced organization and training dynamics of the starch granules in the hydrogel matrix. These dynamic behaviors enable multiple tissue-like properties such as programmability, anisotropy, strain-stiffening, mechanochemistry, and self-healability. [Display omitted] •Granular material-based hydrogel composites display tissue-like behaviors•Synchrotron-based tools reveal the structures and dynamics of starch granules•The organization of starch granules can be mechanically programmed for memory devices•Dynamic hydrogen bonding and granular interactions are key to the tissue-like behaviors Biological tissues exhibit dynamic and multiscale architectures of dense cellular ensembles and extracellular matrices (ECMs). However, cell-like building blocks that display coordinated dynamic responses are hard to find, a challenge that has prevented synthetic materials from fully recapitulating tissue-like behaviors. In our work, we design a hybrid material system featuring cell-like granules embedded in ECM-like hydrogel matrices. We report that this composite readily displays tissue-like properties, including strain-stiffening, anisotropy, programmability, mechanochemistry, and self-healability. By using several in situ characterization tools, we attribute the tissue-like behaviors to mechanically induced organization of the starch granules in the hydrogel matrix. The fundamental insights gleaned from our study could also promise future development of adaptive metamaterials used for switches, sensors, actuators, and robotics, whose functions can go beyond those of natural systems. Living tissues contain dense cellular ensembles and extracellular matrices (ECMs). Despite extensive efforts in the biomimetics field to develop