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Living active collectives have evolved with remarkable self-patterning ability to meet the physical and biological constraints for growth and survival. However, how complex multicellular patterns emerge from a single founder cell remains elusive. Here, by recourse to an agent-based model, we track the three-dimensional (3D) morphodynamics and cell orientational order of growing bacterial biofilms encased by agarose gels. Confined growth causes spatiotemporally heterogeneous stress buildup in the biofilm. High hydrostatic and low shear stresses at the core of the biofilm promote viscous-to-elastic transition and randomize cell packing, whereas the opposite stress state near the gel-cell interface drives nematic ordering with a time delay inherent to shear stress relaxation. Overall, stress anisotropy spatiotemporally coincides with nematic order in the confined biofilms, suggesting an anisotropic-stress-driven ordering mechanism. The strong reciprocity between stress anisotropy and cell ordering inspires innovative 3D mechano-lithography of living active collectives for a variety of environmental and biomedical applications.

Active nematics are the nonequilibrium analog of passive liquid crystals in which anisotropic units consume free energy to drive emergent behavior. Similar to liquid crystal (LC) molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions; however, unlike passive liquid crystals, active nematics, such as those composed of living matter, have the potential to regulate their boundaries through self-generated stresses. Here, using bacterial biofilms confined by a hydrogel as a model system, we show how a three-dimensional, living nematic can actively shape itself and its boundary in order to regulate its internal architecture through growth-induced stresses. We show that biofilms exhibit a sharp transition in shape from domes to lenses upon changing environmental stiffness or cell-substrate friction, which is explained by a theoretical model considering the competition between confinement and interfacial forces. The growth mode defines the progression of the boundary, which in turn determines the trajectories and spatial distribution of cell lineages. We further demonstrate that the evolving boundary defines the orientational ordering of cells and the emergence of topological defects in the interior of the biofilm. Our findings reveal novel self-organization phenomena in confined active matter and provide strategies for guiding the development of programmed microbial consortia with emergent material properties.

In growing active matter systems, a large collection of engineered or living autonomous units metabolize free energy and create order at different length scales as they proliferate and migrate collectively. One such example is bacterial biofilms, which are surface-attached aggregates of bacterial cells embedded in an extracellular matrix. However, how bacterial growth coordinates with cell-surface interactions to create distinctive, long-range order in biofilms remains elusive. Here we report a collective cell reorientation cascade in growing Vibrio cholerae biofilms, leading to a differentially ordered, spatiotemporally coupled core-rim structure reminiscent of a blooming aster. Cell verticalization in the core generates differential growth that drives radial alignment of the cells in the rim, while the radially aligned rim in turn generates compressive stresses that expand the verticalized core. Such self-patterning disappears in adhesion-less mutants but can be restored through opto-manipulation of growth. Agent-based simulations and two-phase active nematic modeling reveal the strong interdependence of the driving forces for the differential ordering. Our findings provide insight into the collective cell patterning in bacterial communities and engineering of phenotypes and functions of living active matter.

One of the most celebrated contributions to the study of the mechanical behavior of materials is due to J.D. Eshelby, who in the late 50s revolutionized our understanding of the elastic stress and strain fields due to an ellipsoidal inclusion/inhomogeneity that undergoes a transformation of shape and size. While Eshelby's work laid the foundation for significant advancements in various fields, including fracture mechanics, theory of phase transitions, and homogenization methods, its extension into the range of large deformations, and to situations in which the material can actively reorganize in response to the finite transformation strain, is in a nascent state. Beyond the theoretical difficulties imposed by highly nonlinear material response, a major hindrance has been the absence of experimental observations that can elucidate the intricacies that arise in this regime. To address this limitation, our experimental observations reveal the key morphogenesis steps of Vibrio cholerae biofilms embedded in hydrogels, as they grow by four orders of magnitude from their initial size. Using the biofilm growth as a case study, our theoretical model considers various growth scenarios and employs two different and complimentary methods -- a minimal analytical model and finite element computations -- to obtain approximate equilibrium solutions. A particular emphasis is put on determining the natural growth path of an inclusion that optimizes its shape in response to the confinement, and the onset of damage in the matrix, which together explain the observed behavior of biofilms. Beyond bacterial biofilms, this work sheds light on the role of mechanics in determining the morphogenesis pathways of confined growing bodies and thus applies to a broad range of phenomena that are ubiquitous in both natural and engineered material systems., Comment: 35 pages, 14 figures, 1 appendix figure

Metamaterials achieve unprecedented properties from designed architected structures. However, they are often constructed from a single repeating building block that exhibits monotonic shape changes with single degree of freedom, thereby leading to specific spatial forms and limited reconfigurability. Here we introduce a transformable three-dimensional modular kirigami with multiple degrees of freedom that could reconfigure into versatile distinct daughter building blocks. Consequently, the combinatorial and spatial modular assembly of these building blocks could create a wealth of reconfigurable architected materials with diverse structures and unique properties, including reconfigurable 1D periodic column-like materials with bifurcated states, 2D lattice-like architected materials with phase transition of chirality, as well as 3D quasiperiodic yet frustration-free multilayered architected materials in a long-range order with programmable deformation modes. Our strategy opens an avenue to design a new class of modular reconfigurable metamaterials that are reprogrammable and reusable for potential multifunctionality in architectural, phononic, mechanical, and robotic applications.

Climbing soft robots are of tremendous interest in both science and engineering due to their potential applications in intelligent surveillance, inspection, maintenance, and detection under environments away from the ground. The challenge lies in the design of a fast, robust, switchable adhesion actuator to easily attach and detach the vertical surfaces. Here, we propose a new design of pneumatic-actuated bioinspired soft adhesion actuator working both on ground and under water. It is composed of extremely soft bilayer structures with an embedded spiral pneumatic channel resting on top of a base layer with a cavity. Rather than the traditional way of directly pumping air out of the cavity for suction in hard polymer-based adhesion actuator, we inflate air into the top spiral channel to deform into a stable 3D domed shape for achieving negative pressure in the cavity. The characterization of the maximum shear adhesion force of the proposed soft adhesion actuator shows strong and rapid reversible adhesion on multiple types of smooth and semi-smooth surfaces. Based on the switchable adhesion actuator, we design and fabricate a novel load-carrying amphibious climbing soft robot (ACSR) by combining with a soft bending actuator. We demonstrate that it can operate on a wide range of foreign horizontal and vertical surfaces including dry, wet, slippery, smooth, and semi-smooth ones on ground and also under water with certain load-carrying capability. We show that the vertical climbing speed can reach about 286 mm/min (1.6 body length/min) while carrying over 200g object (over 5 times the weight of ACSR itself) during climbing on ground and under water. This research could largely push the boundaries of soft robot capabilities and multifunctionality in window cleaning and underwater inspection under harsh environment.