Active nematic order and dynamic lane formation of microtubules driven by membrane-bound diffusing motors
| Autor: | Fereshteh L. Memarian, Joseph D. Lopes, Fabian Jan Schwarzendahl, Madhuvanthi Guruprasad Athani, Niranjan Sarpangala, Ajay Gopinathan, Daniel A. Beller, Kinjal Dasbiswas, Linda S. Hirst |
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| Rok vydání: | 2021 |
| Předmět: |
Microscopy
Multidisciplinary Swine Physics 1.1 Normal biological development and functioning Lipid Bilayers Kinesins biopolymers Bioengineering Microtubules Fluorescence Biomechanical Phenomena Diffusion Kinetics Microscopy Fluorescence Tubulin Underpinning research active nematic Physical Sciences Animals liquid crystal active matter |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America, vol 118, iss 52 Proceedings of the National Academy of Sciences of the United States of America |
| Popis: | Significance Active nematics are ordered liquid crystalline fluids that exhibit spontaneous persistent flows and collective dynamics. The development of motile biopolymer systems inspired by nature has recently attracted considerable attention to out-of-equilibrium soft materials. We report the formation of an active nematic in which microtubules are propelled by kinesin motors coupled to a lipid membrane substrate. The system exhibits apolar order in a globally aligned nematic phase and locally ordered dynamic lanes. Use of a fluid substrate represents a significant advance for active matter as it allows for spatial re-organization of motors, which generate force, in response to the dynamics of the aligning microtubules. This self-organized feedback mechanism may have implications in vivo and for engineering efficient dynamic and reconfigurable materials. Dynamic lane formation and long-range active nematic alignment are reported using a geometry in which kinesin motors are directly coupled to a lipid bilayer, allowing for in-plane motor diffusion during microtubule gliding. We use fluorescence microscopy to image protein distributions in and below the dense two-dimensional microtubule layer, revealing evidence of diffusion-enabled kinesin restructuring within the fluid membrane substrate as microtubules collectively glide above. We find that the lipid membrane acts to promote filament–filament alignment within the gliding layer, enhancing the formation of a globally aligned active nematic state. We also report the emergence of an intermediate, locally ordered state in which apolar dynamic lanes of nematically aligned microtubules migrate across the substrate. To understand this emergent behavior, we implement a continuum model obtained from coarse graining a collection of self-propelled rods, with propulsion set by the local motor kinetics. Tuning the microtubule and kinesin concentrations as well as active propulsion in these simulations reveals that increasing motor activity promotes dynamic nematic lane formation. Simulations and experiments show that, following fluid bilayer substrate mediated spatial motor restructuring, the total motor concentration becomes enriched below the microtubule lanes that they drive, with the feedback leading to more dynamic lanes. Our results have implications for membrane-coupled active nematics in vivo as well as for engineering dynamic and reconfigurable materials where the structural elements and power sources can dynamically colocalize, enabling efficient mechanical work. |
| Databáze: | OpenAIRE |
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