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      Controlling Organization and Forces in Active Matter Through Optically-Defined Boundaries

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          Abstract

          Living systems are capable of locomotion, reconfiguration, and replication. To perform these tasks, cells spatiotemporally coordinate the interactions of force-generating, “active” molecules that create and manipulate non-equilibrium structures and force fields that span up to millimeter length scales [ 1- 3]. Experimental active matter systems of biological or synthetic molecules are capable of spontaneously organizing into structures [ 4, 5] and generating global flows [ 6- 9]. However, these experimental systems lack the spatiotemporal control found in cells, limiting their utility for studying non-equilibrium phenomena and bioinspired engineering. Here, we uncover non-equilibrium phenomena and principles by optically controlling structures and fluid flow in an engineered system of active biomolecules. Our engineered system consists of purified microtubules and light-activatable motor proteins that crosslink and organize microtubules into distinct structures upon illumination. We develop basic operations, defined as sets of light patterns, to create, move, and merge microtubule structures. By composing these basic operations, we are able to create microtubule networks that span several hundred microns in length and contract at speeds up to an order of magnitude faster than the speed of an individual motor. We manipulate these contractile networks to generate and sculpt persistent fluid flows. The principles of boundary-mediated control we uncover may be used to study emergent cellular structures and forces and to develop programmable active matter devices.

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          Most cited references16

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          Mechanical integration of actin and adhesion dynamics in cell migration.

          Directed cell migration is a physical process that requires dramatic changes in cell shape and adhesion to the extracellular matrix. For efficient movement, these processes must be spatiotemporally coordinated. To a large degree, the morphological changes and physical forces that occur during migration are generated by a dynamic filamentous actin (F-actin) cytoskeleton. Adhesion is regulated by dynamic assemblies of structural and signaling proteins that couple the F-actin cytoskeleton to the extracellular matrix. Here, we review current knowledge of the dynamic organization of the F-actin cytoskeleton in cell migration and the regulation of focal adhesion assembly and disassembly with an emphasis on how mechanical and biochemical signaling between these two systems regulate the coordination of physical processes in cell migration.
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            Emergence of macroscopic directed motion in populations of motile colloids

            From the formation of animal flocks to the emergence of coordinated motion in bacterial swarms, populations of motile organisms at all scales display coherent collective motion. This consistent behaviour strongly contrasts with the difference in communication abilities between the individuals. On the basis of this universal feature, it has been proposed that alignment rules at the individual level could solely account for the emergence of unidirectional motion at the group level. This hypothesis has been supported by agent-based simulations. However, more complex collective behaviours have been systematically found in experiments, including the formation of vortices, fluctuating swarms, clustering and swirling. All these (living and man-made) model systems (bacteria, biofilaments and molecular motors, shaken grains and reactive colloids) predominantly rely on actual collisions to generate collective motion. As a result, the potential local alignment rules are entangled with more complex, and often unknown, interactions. The large-scale behaviour of the populations therefore strongly depends on these uncontrolled microscopic couplings, which are extremely challenging to measure and describe theoretically. Here we report that dilute populations of millions of colloidal rolling particles self-organize to achieve coherent motion in a unique direction, with very few density and velocity fluctuations. Quantitatively identifying the microscopic interactions between the rollers allows a theoretical description of this polar-liquid state. Comparison of the theory with experiment suggests that hydrodynamic interactions promote the emergence of collective motion either in the form of a single macroscopic 'flock', at low densities, or in that of a homogenous polar phase, at higher densities. Furthermore, hydrodynamics protects the polar-liquid state from the giant density fluctuations that were hitherto considered the hallmark of populations of self-propelled particles. Our experiments demonstrate that genuine physical interactions at the individual level are sufficient to set homogeneous active populations into stable directed motion.
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              Fluid dynamics and noise in bacterial cell-cell and cell-surface scattering

              Bacterial processes ranging from gene expression to motility and biofilm formation are constantly challenged by internal and external noise. While the importance of stochastic fluctuations has been appreciated for chemotaxis, it is currently believed that deterministic long-range fluid dynamical effects govern cell-cell and cell-surface scattering-the elementary events that lead to swarming and collective swimming in active suspensions and to the formation of biofilms. Here, we report direct measurements of the bacterial flow field generated by individual swimming Escherichia coli both far from and near to a solid surface. These experiments allowed us to examine the relative importance of fluid dynamics and rotational diffusion for bacteria. For cell-cell interactions it is shown that thermal and intrinsic stochasticity drown the effects of long-range fluid dynamics, implying that physical interactions between bacteria are determined by steric collisions and near-field lubrication forces. This dominance of short-range forces closely links collective motion in bacterial suspensions to self-organization in driven granular systems, assemblages of biofilaments, and animal flocks. For the scattering of bacteria with surfaces, long-range fluid dynamical interactions are also shown to be negligible before collisions; however, once the bacterium swims along the surface within a few microns after an aligning collision, hydrodynamic effects can contribute to the experimentally observed, long residence times. Because these results are based on purely mechanical properties, they apply to a wide range of microorganisms.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                26 June 2019
                07 August 2019
                August 2019
                07 February 2020
                : 572
                : 7768
                : 224-229
                Affiliations
                [1 ]California Institute of Technology, Pasadena, California, 91125, USA.
                [2 ]Division of Biology and Biological Engineering
                [3 ]Department of Applied Physics
                [4 ]Department of Physics
                Author notes

                Author Contributions T.D.R., H.L., R.P, and M.T. conceived the experiments and interpreted the results. T.D.R., H.L., R.A.B., Z.Q., and M.T. wrote the manuscript. T.D.R. designed and cloned iLID motor fusion constructs. T.D.R., H.L., and R.A.B. performed protein purification. T.D.R. and H.L. designed, performed, and analyzed active matter experiments. Z.Q. analyzed and modeled flow data and tracked trajectories of moving asters. R.A.B. performed and analyzed gliding assays. All authors discussed results and commented on the manuscript.

                Article
                NIHMS1531196
                10.1038/s41586-019-1447-1
                6719720
                31391558
                ef3b88a6-7d87-4dae-8dee-3604c6011f78

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