Abstract
Biological systems control ambient fluids through the selforganization of active protein structures, including flagella, cilia, and cytoskeletal networks. Selforganization of protein components enables the control and modulation of fluid flow fields on micron scales, however, the physical principles underlying the organization and control of activematterdriven fluid flows are poorly understood. Here, we use an opticallycontrolled activematter system composed of microtubule filaments and lightswitchable kinesin motor proteins to analyze the emergence of persistent flow fields. Using light, we form contractile microtubule networks of varying size and shape, and demonstrate that the geometry of microtubule flux at the corners of contracting microtubule networks predicts the architecture of fluid flow fields across network geometries through a simple point force model. Our work provides a foundation for programming microscopic fluid flows with controllable active matter and could enable the engineering of versatile and dynamic microfluidic devices.
Introduction
Control of fluids is essential for biological processes, including motility and material transport across the cell, tissue, and organismal scales of organization^{1,2,3,4,5,6}. For example, within cells, cytoskeletal networks composed of filaments and motor proteins induce cytoplasmic flows or streams that drive processes ranging from chloroplast transport in algae to the recycling of motility proteins during eukaryotic chemotaxis^{1,7,8}. The key conceptual challenge is to understand how selforganized “active” protein structures like cilia and cytoskeletal networks convert chemical energy into mechanical forces at molecular scales to generate and modulate fluid flow fields on micron length scales. Here, active structures refer to systems consuming chemical energy to generate forces through selforganization. In contrast to such systems, in a conventional systems like a pipe or propeller, fluid flows emerge due to the macroscopic forces applied to boundary conditions^{9,10,11}. However, in cellular flow control, force fields emerge from within the fluid itself through the action and molecular selforganization of motor and filament proteins. Protein components both induce and respond to fluid flows, so that flows alter the distribution of force and material over time.
Simplified active matter systems allow the analysis of selforganized fluid control as well as providing a potential platform for technology development. Active matter systems composed of purified filament and motor proteins can generate nonequilibrium, selforganized structures, including microtubules asters,^{12,13,14} that generate spontaneous fluid flows^{10,15,16,17,18}. However, these fluid flows are typically disorganized and chaotic. Artificial boundaries can be applied to confine active systems experimentally and organize fluid flows by imposing boundary conditions^{10}. Recently, we developed an optically controlled active matter system^{19} (Fig. 1a) composed of microtubules and engineered kinesin motor proteins, where fluid flows can be generated and modulated with light, with organized fluid flows emerging through optically guided selforganization of microtubules and motors into networks that induce flow in ambient fluids. However, while we can demonstrate that the geometry of the light inputs into the system alters patterns of fluid flow, we lack a predictive understanding of how flow fields become spontaneously selforganized through active matter dynamics.
In this paper, we apply our lightswitchable active matter system to analyze the emergence of selforganized flow fields within opticallycontrolled active matter. We generate microtubule networks of different sizes and shapes that induce persistent fluid flows. By using light to modulate the geometry of microtubulemotor networks, we demonstrate that selforganized flow fields emerge through dynamic feedback between microtubule network contraction and fluiddriven mass transport. Fluidnetwork interactions generate persistent microtubule flux at the corners of contracting, polygonal microtubule networks. The geometry of microtubule flux at the network boundary predicts the steadystate flow field for a wide range of polygonal microtubule network geometries. We develop a simple theoretical model based upon boundary point forces that predicts the qualitative and quantitative flow fields generated by polygonal microtubule network contraction. The boundary force model provides a formal and integrated framework for predicting flow fields and allows quantitative comparison with experimental data, thus extending prior work^{19}. Our boundary force model reveals that the flow field generated by microtubule networks spanning hundreds of microns can be understood as the flow field generated by simple pointforce solutions of Stokes equation where point forces pointing towards the center, scaling in amplitude with the distance to the center, are arranged on the corners of a contracting microtubule network. Our results reveal a dynamic mechanism of fluid flow generation in active microtubule networks and provide a modeling framework to predict the flowfield architecture from an active mattergenerated boundary condition.
Results
Microtubule network contraction induces mass transport and persistent fluid flows
Our active matter system consists of stabilized microtubule filaments and kinesin motor proteins which, when modulated by light, induce fluid flow (Fig. 1a; Methods). The engineered kinesin motor protein reversibly crosslink under illumination (Fig. 1a) inducing interactions between motors on neighboring microtubules leading to microtubule network formation, contraction, and the generation of persistent fluid flows. In previous work^{19}, we described the emergence of activematterdriven fluid flows within the experimental system. However, the mechanism of flow generation and modulation has remained poorly understood and quantitative comparisons between theory and experiment have not been previously reported.
We developed an experimental platform^{19} that allows us to optically induce and track both microtubule and flowfield dynamics (Supplementary Methods 2). Our experimental system (Fig. 1b) uses a conventional fluorescence microscope and a digital light projector to control sample illumination. We tracked microtubule dynamics via a fluorescent microtubule dye and, simultaneously, introduced micronsized tracer particles to quantify the flowfield architecture through particle tracking. The experimental system allows us to induce microtubule networks of differing sizes and shape with light and to track the dynamics of the active matterfluid system as the fluid flows emerge.
We analyzed the fluid and microtubule dynamics induced by optical activation of a 600 µm square region (Fig. 1c–e, Supplementary Methods 3 and 4). Light activationinduced persistent fluid flows through the formation of a microtubule network that spontaneously contracted to its center of mass. As the microtubule network contracted, it induced fluid flows within the bulk microtubules (Fig. 1d, cyan arrows) outside of the lightactivated region, as quantified by particle image velocimetry (PIV) (Supplementary Fig. 1). The background flows lead to an influx of microtubules along the corners of the contracting microtubule network leading to an increase in integrated microtubule density within the illuminated region over time (Supplementary Fig. 2, Supplementary Note 1). Persistent microtubule flux at the network corners was maintained for more than 15 min due to a persistent influx of microtubules from the background solution into the lightactivated region (Supplementary Movie 1). We observed similar microtubule flux in simulations of contracting square microtubule networks (Methods). In these simulations, we treated each position within a contracting microtubule network as a point force whose amplitude is set by the contractile velocity of the network^{20,21}. Each point force acts as a source for fluid flow due to Stokesian fluid dynamics^{22,23} (Fig. 1f, g). In these simulations, microtubule network contractions generated a fluid flow field that leads to inflows of even more particles at the network corners.
Experimentally, the emergence of persistent microtubule flux at the corners of the contracting network coincides with the emergence of steadystate fluid inflows (Fig. 1h) along the corners of the square and fluid outflows along the edges of the activation region. In addition, the fluid flow field contains four pairs of approximately 100 µm (in radius) centers of vorticity oriented along each arm of the microtubule structure. Broadly, fluid inflows align with the persistent influx of microtubules along the microtubule network corners. The observation is consistent with a model where microtubule influx along the corners of the network act as force sources that generate the fluid flows.
Microtubule network boundary geometry determines the organization of the flow field
We found that the geometry of the microtubule network boundary alone is sufficient to determine the architecture of the microtubule influx as well and the fluid flow fields for square microtubule networks. To analyze the role of the microtubule flux along the boundary of the microtubule network in generating and organizing fluid flows, we created a series of 400 µm microtubule networks with a square boundary where we introduced square cavities into the center of the network (Fig. 2a–d, Supplementary Figs. 2 and 3, Supplementary Note 2). In total, we created four different networks with cavities ranging from 100 to 360 µm (25% and 90%) in length. By altering the distribution of active material and the network topology, the hollow networks allowed us to examine the relative contribution of the network boundary and interior to the generation of the fluid flow field.
The hollow square networks execute a similar process of microtubule network formation, network contraction, and boundary linking, leading to persistent microtubule flux at network corners. For the hollow shapes, the contractile network adopts the geometry of the light pattern, so that network itself contains a square hole throughout the network contraction (Fig. 2a). In each case, the contracting network generates a diagonal distribution of microtubule flux at the corners of the illumination region (Fig. 2a, c, Supplementary Figs. 3 and 4). The microtubule distribution observed for the hollow networks is qualitatively similar to the material distribution generated by the contraction of the intact square network. Like the intact square network in Fig. 1d, the hollow networks generate a persistent microtubules influx in the form of arms along the network corners (Supplementary Movies 2–5).
The hollow squares also generate persistent fluid flow fields (Fig. 2b, d) that are very similar to the intact square networks in terms of their qualitative and quantitative features. Like the filled square network, hollownetworkinduced fluid flow fields exhibited diagonal inflows, edge outflows, and a series of vortex pairs. The vortex pairs across all networks were quantitatively comparable in their size and location (Fig. 2e). We quantified the position of vortices by fitting the vorticity (∇ × v) with a Gaussian mixture model and extracting the centroid and shape of each vorticity peak or valley. The extracted vorticity peaks across the five different networks had centroid centers lying within 10 µm of one another (Fig. 2e). Further, the maximum of the fluid velocity was approximately 1 µm s^{−}^{1} along the inflow and 0.7 µm s^{−1} along the outflow (Fig. 2f), and the maximal and minimal fluid speeds agree across the five networks to within the variation measured for replicates of individual networks.
The distribution of microtubule density and flux at the corners of the applied light pattern was similar for the four cavity networks and the full square network. This finding suggests that the microtubule flux at the corners of the contracting networks plays a central role in determining the architecture of the generated fluid flows. In addition, supporting the notion of the flow being driven by the microtubule flux, circular light patterns generate networks that exhibit radial contraction without persistent fluid flow or microtubule arms (Supplementary Fig. 5, Supplementary Note 3).
The boundary force model predicts flowfield geometry
Based on our analysis of the flow fields induced by the hollow square networks, we developed a simple mathematical model to predict the architecture of fluid flow fields generated by contracting microtubule networks using boundary forces alone. The boundary force model formalizes and extends previous work^{19} in which we proposed a qualitative model for fluid flows by placing Stokeslets at all locations within a contracting microtubule network. In our boundary force model, the microtubule influx at the corners of the network generates the force that is transferred to the fluid to induce flow. Our model is based upon the following observations. First, microtubule network contraction leads to diagonal inflows of activated microtubules at the corners of the contracting microtubule network. Second, networks with a square boundary but distinctly different internal structures induce nearly identical patterns of fluid flow. Third, moving microtubules are known to act on their ambient fluid as local point sources of force. Therefore, we propose that the force generated by active microtubule flux along the corners of the contracting network determines the architecture of the induced flow field. In what follows we develop the boundary force model, and then demonstrate that the model allows flow field predictions that can be compared quantitatively with experimental data. In addition to enabling quantitative comparison the boundary force model provides insight into how key features of the flow fields, including the position of vortices, are determined by active matter network geometry.
In our boundary force model, the fluid is considered in the incompressible Stokesian limit (valid at low Reynolds numbers) so that the fluid velocity v obeys the Stokes equation
where μ is the fluid viscosity, p is the pressure, and f is the force field exerted by the active matter. The hypothesis is that for convex polygonal illumination patterns the geometry of the corners determines the flow. In this model, it means f to be nonvanishing only in the corners. Therefore, f is a sum of fourpoint forces directed toward the center of the shape for a rectangular pattern illumination, due to symmetry. These properties determine Eq. (1) up to a trivial rescaling of all quantities since Eq. (1) is linear.
Due to the linearity of Eq. (1), the fundamental solution could be used to obtain the flow field for free boundary conditions^{24}. However, incorporating more general boundary conditions in this solution method can be challenging^{25}. In this particular case, two sets of boundary conditions have to be imposed. The first set models the noslip condition at the limits of our fluid flow cell, while the second set describes the inhibition of fluid flow due to the jamming of microtubules. This latter boundary condition is achieved by imposing an area with no slip at its boundary at the center of the activated area, with the same shape as the activation area, but with half of the (linear) dimensions. Since these boundary conditions are difficult to treat with the fundamental solution, finiteelement methods (FEM) simulations were used, based on FEniCS^{26}. It should be noted that due to the limitations of FEM, point forces are spread out over a finite kernel (see Supplementary Methods 6).
Boundary force model captures aspectratio induced flowfield transitions for rectangular networks
For square networks, we found that the model predicted a flow field with fluid inflows along the network diagonal and outflows along the edges leading to pairs of vortices along the corners of the networks (Fig. 3a–d, top row). In general, there is a close resemblance between the qualitative features of the experiment and theory.
We, therefore, generalized our model to predict the flow generated by rectangular networks with a range of different aspect ratios. For rectangular networks, the model predicted the correct number and position of fluid vortices (Fig. 3c). In the rectangular geometries, we experimentally observe a crossover from inflow to outflow along the long axis of the rectangle for increasing aspect ratio. Moreover, the emergence of new vortices left and right of the activated area can be well observed in the streamlines for both the experiment and theory. It is even more apparent in the vorticity, shown in the background of the figures, demonstrating the resemblance between theory and experiment.
The vorticity was further analyzed by comparing the experiment to the theory directly by fitting with a mixture of Gaussians. Comparison of their centers and their extent revealed a significant overlap between experimental and simulated centers of vorticity (Fig. 3d), with the average distance between experimental data and simulation being approximately 46 µm, which is much smaller than the typical extent of the activated region of 400 µm.
On an intuitive level, the simulated flow field can be understood as emerging from twodimensional Stokeslets placed only at the corners of the network. Therefore, the vortices that arise at the corner of the network can be understood as emerging due to the vortex pair around the fundamental Stokeslet solution to Stokes equation for a point force^{27}. This intuitive picture can be used to address the qualitative disagreement between theory and experiment, where the peaks of vorticity do not align with the center of circulation in the simulation results, but they do in the experiment. In the simulation, the forces were (almost) pointlike so that the vorticity is concentrated along the point force, as expected for Stokeslets. In contrast, in the experiment, the forces are spread out over the width of the “arm” linking the background fluid to the contractile network. The finite extent of this arm pushes the vorticity peaks apart, making them align with the center of circulation.
Finally, while the number of vortex cores and their location was our primary method of comparing the simulation results with the experiment, the fluid velocities could also be compared directly. We chose to compare along the long axis of the rectangle because the fluid velocity exhibits a (distancedependent) crossover behavior from inflow to outflow for increasing aspect ratio. Qualitatively, we show that this crossover is seen in both experiment and simulation (Fig. 3e–g). However, a direct comparison should be viewed with caution, because the details of the crossover, such as the location of the inversion point at a fixed aspect ratio, depend on details of the simulation, such as the size of the inner jamming region, and are difficult to locate precisely in the experiment.
The boundary force description predicts flow field induced by polygonal networks
While the rectangular activation area provides a useful test case for the model, we wanted to develop a more general framework able to predict the flow fields generated by a range of polygonal shapes. In analogy, we introduced point forces on the corners of the polygonal light pattern (Supplementary Fig. 6). In each case, we found that the corner force description was sufficient to determine the number and location of fluid vortices as well as the orientation of fluid flows.
Regular triangles and hexagons were considered (Fig. 4a): Due to symmetry, forces are in the corners, pointing towards the center, and each force amplitude is the same (Supplementary Movies 6–8). An excellent qualitative agreement between theory and experiment was observed as seen in the Gaussian mixture model comparison (Fig. 4b–d). The locations of the vorticity peaks and valleys overlap well between the experimental observation and the simulation. Hence, these comparisons demonstrate that our model can generalize to regular polygons. It should be noted that even circular activation patterns can be understood in this manner, by considering them as regular polygons with a large number of corners. Our model indeed correctly predicts the absence of flow even in this case (Supplementary Fig. 7, Supplementary Note 4).
A nonregular polygon was also considered, through an isosceles triangle (Supplementary Movie 8). Because the polygon is no longer regular, there is no longer a symmetry reason for all forces to be equally strong. While we still assume that the forces point towards the center of the activated area, we hypothesized that their amplitudes scaled linearly with distance to the center. In other words, corners farther away from the center induce a stronger fluid flow, based on published experimental results^{19,20}. It should be noted that one could additionally hypothesize a force scaling dependent on the corner angle, having the largest forces for angles closer to 0° and vanishing for 180°. However, for this paper we decided to use exclusively the simpler distance scaling, since a good agreement can be observed between the experiment and the model, therefore, providing compelling evidence that our description can also be applied to nonregular polygons (Fig. 4a–d, middle row).
Discussion
In this work, we analyze the emergence of selforganized fluid flows in an optically controlled microtubulemotor active matter system in vitro where the geometry of the active matterinduced flow field can be modulated by an applied light pattern. We demonstrate that activematter–fluid interactions lead to a selforganized flux of microtubules along the corners of polygonal microtubule networks. By modeling these fluxes as point forces, we are able to predict the architecture of persistent flow fields generated by a range of polygonal network geometries. Our model shows that the distribution of forces on the boundary of an active structure is sufficient to predict the flow field generated by the active matter system. The corner force field itself emerges through a selforganization process driven by microtubule network contraction and mass transport. Therefore, our model reveals how selforganized microtubule flux can control the geometry of active matterdriven fluid flows.
In our model, microtubule flux along the boundary of the active matter system plays an essential role in determining the induced flow field. The persistent, steadystate flow structure observed in this work reveals the role of force and material localization in activematterdriven fluid flows. Our experimental system spontaneously generates organized flow fields that resemble extensional fluid flow fields^{28}. Compared with the previous model we proposed to predict the flow field generated by the same system^{19}, the current model describes the flow architecture more accurately and through a simplified physical mechanism that only involves the network boundary. Indeed, the emergence and location of the vortices in the experiments are only correctly predicted by our model, mainly as a result of our ability to incorporate physically accurate boundary conditions. Solving the Stokes equation directly, as opposed to working with Stokeslet superpositions, enables us to explore the fundamental principles of the flow field induced by the active matterfluid interaction. We can understand vortices as arising due to the vortex pairs that emerge around the fundamental pointforce solution to Stokes equation^{27}. The experiments with hollow squares confirm the hypothesis that the corners of the optically defined boundary determine the flow architecture, and the forces can be reduced to a single localized force in the corner in contrast to a series of forces along the diagonal. It should be noted, that our model describes the steadystate flow field well, but does not describe the transient dynamics of the system. It will be very interesting for future work to analyze the coupled active matter–fluid dynamics, which could reveal an interesting force scaling with the distance from the centroid, the corner angles, and curvature radii^{29}.
Previous work on activematterdriven fluid flows has observed that active nematics composed of microtubules and motor proteins generate spontaneous but chaotic fluid flows fields^{15,16}. Furthermore, in these systems, confinement of the nematic within passive fabricated boundary leads to the organization of chaotic flows^{1,17}. In our system, the selforganization of microtubule density within the active matter fluid system itself generates organized flow fields. The boundary forces used in our predictive model emerge experimentally through the selforganization of microtubule “arms” at the corners of our applied light pattern. Therefore, our work reveals a mechanism of selforganized flow modulation and demonstrates how organized flows can emerge in the active matter without passive, fabricated boundaries. Indeed, cells and microorganisms use both physical and chemical mechanisms to control the shape of active matter networks to modulate fluid flows^{22,30}.
We explored a limited set of flow patterns generated by convex, polygonal network geometries. It will be important, in future work, to explore the range of fluid fields that can be generated by exploring a wider range of geometries, considering possible history dependence, and combining flow fields generated by different illumination patterns with superposition. Further, the organized flow field is a potential platform for building micromachines. For example, it has been shown that microscopic gears can be driven by bacterial suspensions to collect mechanical energy^{31,32}, and a similar device could be combined with the microtubule–kinesin system and driven by the fluid flow as an active switch.
Methods
The active matter system consists of stabilized microtubules, kinesin motors (constructed with the lightinduced heterodimer system), and a necessary energy mix. We note that, in our system, kinesin motor linking leads to contractile microtubule network dynamics^{19,20} In contrast, in a related system with a depletion agent (PEG)^{15}, the motor–microtubule system generates extensile dynamics^{15,33}.
All ingredients and buffer preparation protocols are documented in a previous paper from our group^{19} and we follow the exact same procedure in this study using the aster assay. Inert particles with a 1 µm diameter are suspended in the system for flow field measurement purposes. The sample chambers are made by sandwiching precut Parafilm M by coated slides and coverslips^{19,34}. The measured depth of the chamber is approximately 70 µm.
The experiment is conducted on a conventional microscope (Nikon TE2000) with tenfold magnification. We customize the system by adding a programmable digital light projector (EKB Technologies DLP LightCrafter E4500 MKII Fiber Couple), which is used to activate the kinesin motors with the projected polygonal patterns. The digital light projector chip is illuminated by the 470 nm LED (ThorLabs M470L3) to project polygonal patterns and activate the crosslinking between motors. The fluorescently labeled microtubules are illuminated by 660 nm light and imaged with a digital camera (FliR BFLYU323S6MC). The system is controlled with the MicroManager software package (https://micromanager.org/) on a computer.
The microtubule flow field is estimated using PIV by analyzing the images at 660 nm. The PIV is performed by a custom code written in Matlab^{35} to measure the velocity field of the microtubule contraction dynamics (within the illumination region) and microtubule movements alongside the fluid flow (outside the illumination region). In particular, the microtubule velocity field is determined through local maximization of the correlation between the warped and the target images.
For the simulation in Fig. 1f, g, active particles are modeled as point forces that generate twodimensional Stokeslets^{27}. The force vectors point toward the center of the contracting network with a magnitude that is proportional to the particle’s distance from the activation area center.
The flow field is measured by first comparing the position of individual inert particles from frame to frame^{36} for the particle displacement with a nearestneighbor algorithm (15 pixels threshold)^{37}. Then the displacement vector field, which is sparse due to the randomness of the particle locations, is grouped within a 30 × 30 pixels consecutive window and averaged over minute 2 to minute 15 of the experiment. The velocity field is calculated by dividing the displacement field by the time interval between frames, 5 s. Finally, the velocity field at each time step of the experiment is calculated and averaged to get the timeaveraged velocity field.
The solution to Eq. (1) with the boundary conditions described in the text was found by employing FEM. In particular, the FeniCS library^{26} was used in our code, which can be found on GitHub: https://github.com/domischi/StokesFEM. Noslip boundary conditions were applied at the upper and lower edge of the simulation cell, as well as in a central region with half the linear size of the activation region. The point forces were spread out over a small region, with onetenth of the size of the activated region. The solution approach further used Taylor–Hoods basis functions and a quadratic meshing. Additional details can be found in Supplementary Methods 6.
Reporting summary
Further information on research design is available in the Nature Research Reporting Summary linked to this article.
Data availability
The data is openly available at https://doi.org/10.22002/D1.1858.
Code availability
The code to reproduce our main findings can be found on the following Github repositories: The FEM code can be found on https://github.com/domischi/StokesFEM and the PIV analysis code is on https://github.com/ShaiShdk/ActiveFlow_PIV.
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Acknowledgements
We acknowledge funding from the Donna and Benjamin M. Rosen Bioengineering Center, Foundational Questions Institute and Fetzer Franklin Fund (through FQXi 1816), The Moore Foundation, The Packard Foundation, and Heritage Medical Research Institute. We thank InnaMarie Strazhnik for the preparation of figures and illustrations. We acknowledge Dr. Guy Riddihough for his editorial assistance with the paper.
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Z.Q., J.J., H.J.L., R.P., and M.T. conceived the project. Z.Q., H.J.L., D.L., and F.Y. performed the experiments. J.J. performed the initial investigations of the model. D.S. developed the theoretical framework and performed the finiteelement simulations. S.S. performed the PIV analysis. E.A. performed the image segmentation analysis. Z.Q., D.S., and M.T. wrote the paper with input from all authors.
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Qu, Z., Schildknecht, D., Shadkhoo, S. et al. Persistent fluid flows defined by active matter boundaries. Commun Phys 4, 198 (2021). https://doi.org/10.1038/s42005021007033
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DOI: https://doi.org/10.1038/s42005021007033
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