Multiscale investigation of the emergent behaviors in biomimetic active matter
Creators: name: Najma, Bibi
Publisher: name: Brandeis University
Year: 2023
Subjects: active matter
asters
FRAP
kinesin
microtubule
PRC1 crosslinker
Biophysics

description: Living cells consist of a myriad of proteins, which form intricate structures that can self-organize in both space and time. These structures are characterized by their dynamic nature and have the ability to sculpt their own architecture. An example of these structures is the cellular cytoskeleton that generates force through the regulation of binding and unbinding kinetics of its molecular building blocks. Cell uses the building blocks of cytoskeleton such as microtubules and molecular motors to perform diverse functions ranging from setting up cytoplasmic flows to generating mechanical forces to drive chromosome segregation. Living cells optimize the transitions between these cytoskeletal states by regulating the length and stability of microtubules, as well as the interaction of ensemble of molecular motors. It is unclear how these protein-scale interactions set the large-scale mechanics of the cytoskeleton and drive various phase transitions.
description: When reconstituted in vitro, these cytoskeletal proteins serve as building blocks to study dynamics and self-organization. Like the cell cytoskeleton, such reconstituted systems are driven away from equilibrium through intricate energy transduction
description: processes. These active systems provide a foundation for integrating biological functionality into the field of materials science. A great challenge would be to realize a minimal active cytoskeleton network using only stabilized microtubules and a single type of motor that exhibits a diverse range of complex dynamics and self-organization. Here, we show that the energy dissipation at microscopic scale due to binding and ATP-powered translocation of highly processive Kinesin-1 K401 motor
description: clusters along stabilized microtubules cascade up into emergent dynamics, including spontaneous extensile deformations and flows, locally contractile asters, and bulk contraction. We show that the self-organization of microtubule networks into distinct emergent structures depends on how the Kinesin-1 K401 We demonstrate that motor clusters have a dual antagonistic role in fluidizing or stiffening of extensile microtubule networks, depending on the ATP concentration. As a result, the emergent active network demonstrates fluid-like bend instability or the solid-like buckling. By combining experiments, continuum theory, and chemical kinetics, we show how to assemble microtubule networks with targeted activity and elasticity by setting the concentrations of molecular motors. We also show that spatiotemporal control of motor activity via light-induced pulses can manipulate the active and elastic stresses in the network, allowing control of the network's fluidity. We also find that clusters of Kinesin-1 K401 motors can trigger extensile to the contractile phase transition in this simple reconstituted system. We explore the microscopic origin of this transition by investigating protein-scale interactions. We correlate bulk structure with motor distribution asymmetry along single microtubule filaments, showing that emergent bulk dynamics are linked to the distribution of processive motor clusters. Uniform distribution results in extensile flows, while end-accumulation leads to aster formation and global contraction. We find depletants, microtubule-specific crosslinkers, and colloidal rods
description: increase nematic alignment, causing the transition from contractile asters to extensile bundles, without impacting motor cluster end-accumulation at the single filament level. Combining experiments and simple scaling arguments, we demonstrate that the extensile-to-contractile transition is akin to a self-assembly process where nematic and polar aligning interactions compete.
description: We further investigate the material properties of aster assemblies resulting from motor-induced active contraction of the microtubule network. These asters demonstrate characteristics that are typically associated with different categories of active matter, including contractile networks and active condensation. Our findings reveal that asters exhibit meso-scale properties that can be either liquid-like or solid-like. Photobleaching experiments showed that these asters undergo an aging process over time, leading to the formation of solid-like or gel-like states with slower internal rearrangement dynamics.
description: Consequently, their fusing ability decreases, and they tend to form clusters. We also found that the aging of asters is directly related to the concentration of crowding agents such as polyethylene glycol (PEG), which modulate the lifetime and fluidity of these asters.
description: Overall, this work demonstrates that precise biochemical and mechanical tuning at the microscopic level can control the robust self-organization of cytoskeletal active materials. These results emphasize the role of cytoskeletal stresses in regulating the self-organization of living matter and pave the way for the rational design and control of active materials. Our findings raise intriguing questions at the intersection of emerging fields such as active matter, the biophysics of the cytoskeleton, and phase separation in cell biology.