Dynamic swarms regulate the morphology and distribution of soft membrane domains.

We study the dynamic structure of lipid domain inclusions embedded within a phase-separated reconstituted lipid bilayer in contact with a swarming flow of gliding filamentous actin. Passive circular domains transition into highly deformed morphologies that continuously elongate, rotate, and pinch off into smaller fragments, leading to a dynamic steady state with ≈23× speedup in the relaxation of the intermediate scattering function compared with passive membrane domains driven by purely thermal forces. To corroborate experimental results, we develop a phase-field model of the lipid domains with two-way coupling to the Toner-Tu equations. We report phase domains that become entrained in the chaotic eddy patterns, with oscillating waves of domains that correlate with the dominant wavelengths of the Toner-Tu flow fields.

Active Surface Flows Accelerate the Coarsening of Lipid Membrane Domains.

Phase separation of multicomponent lipid membranes is characterized by the nucleation and coarsening of circular membrane domains that grow slowly in time as ∼t^{1/3}, following classical theories of coalescence and Ostwald ripening. In this Letter, we study the coarsening kinetics of phase-separating lipid membranes subjected to nonequilibrium forces and flows transmitted by motor-driven gliding actin filaments. We experimentally observe that the activity-induced surface flows trigger rapid coarsening of noncircular membrane domains that grow as ∼t^{2/3}, a 2x acceleration in the growth exponent compared to passive coalescence and Ostwald ripening. We analyze these results by developing analytical theories based on the Smoluchowski coagulation model and the phase field model to predict the domain growth in the presence of active flows. Our Letter demonstrates that active matter forces may be used to control the growth and morphology of membrane domains driven out of equilibrium.

Bio-enabled Engineering of Multifunctional "Living" Surfaces.

Through the magic of "active matter"─matter that converts chemical energy into mechanical work to drive emergent properties─biology solves a myriad of seemingly enormous physical challenges. Using active matter surfaces, for example, our lungs clear an astronomically large number of particulate contaminants that accompany each of the 10,000 L of air we respire per day, thus ensuring that the lungs' gas exchange surfaces remain functional. In this Perspective, we describe our efforts to engineer artificial active surfaces that mimic active matter surfaces in biology. Specifically, we seek to assemble the basic active matter components─mechanical motor, driven constituent, and energy source─to design surfaces that support the continuous operation of molecular sensing, recognition, and exchange. The successful realization of this technology would generate multifunctional, "living" surfaces that combine the dynamic programmability of active matter and the molecular specificity of biological surfaces and apply them to applications in biosensors, chemical diagnostics, and other surface transport and catalytic processes. We describe our recent efforts in bio-enabled engineering of living surfaces through the design of molecular probes to understand and integrate native biological membranes into synthetic materials.

Antibody binding reports spatial heterogeneities in cell membrane organization.

The spatial organization of cell membrane glycoproteins and glycolipids is critical for mediating the binding of ligands, receptors, and macromolecules on the plasma membrane. However, we currently do not have the methods to quantify the spatial heterogeneities of macromolecular crowding on live cell surfaces. In this work, we combine experiment and simulation to report crowding heterogeneities on reconstituted membranes and live cell membranes with nanometer spatial resolution. By quantifying the effective binding affinity of IgG monoclonal antibodies to engineered antigen sensors, we discover sharp gradients in crowding within a few nanometers of the crowded membrane surface. Our measurements on human cancer cells support the hypothesis that raft-like membrane domains exclude bulky membrane proteins and glycoproteins. Our facile and high-throughput method to quantify spatial crowding heterogeneities on live cell membranes may facilitate monoclonal antibody design and provide a mechanistic understanding of plasma membrane biophysical organization.