Swirling Instability of the Microtubule Cytoskeleton

Stein, David B.; Canio, Gabriele De; Lauga, Eric; Shelley, Michael; Goldstein, Raymond E.

doi:10.1103/physrevlett.126.028103

Cited by 33 publications

(18 citation statements)

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“…3 d, indicates fluid speeds from zero to 0.15 μm/s, comparable to velocities observed during cytoplasmic streaming, e.g., ref. 45 . Interestingly, the sharpest gradients in the fluid velocity are found near the edges of the droplets (Figs.…”

Section: Resultsmentioning

confidence: 99%

Sustained enzymatic activity and flow in crowded protein droplets

et al. 2021

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Living cells harvest energy from their environments to drive the chemical processes that enable life. We introduce a minimal system that operates at similar protein concentrations, metabolic densities, and length scales as living cells. This approach takes advantage of the tendency of phase-separated protein droplets to strongly partition enzymes, while presenting minimal barriers to transport of small molecules across their interface. By dispersing these microreactors in a reservoir of substrate-loaded buffer, we achieve steady states at metabolic densities that match those of the hungriest microorganisms. We further demonstrate the formation of steady pH gradients, capable of driving microscopic flows. Our approach enables the investigation of the function of diverse enzymes in environments that mimic cytoplasm, and provides a flexible platform for studying the collective behavior of matter driven far from equilibrium.

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Section: Resultsmentioning

confidence: 99%

Sustained enzymatic activity and flow in crowded protein droplets

et al. 2021

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“…Nanoscale motor proteins, such as kinesin and dynein, convert the cell's chemical energy source, adenosine triphosphate (ATP), into mechanical energy and effectively "walk" along the MT in a processive motion from one end of the MT to the other (1,15,16). Kinesin motor proteins are $60 nm in size and take 8-nm steps in a stochastic, processive motion to transport cargos (i.e., lipid vesicles or organelles) by acting individually or in groups (17)(18)(19). These out-of-equilibrium cellular mechanisms have provided inspiration for a variety of novel in vitro experiments in recent years and biopolymers with molecular motors have been used to create some of the first examples of molecular-scale active phases.…”

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confidence: 99%

Active nematic order and dynamic lane formation of microtubules driven by membrane-bound diffusing motors

Memarian

Lopes

Schwarzendahl

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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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.

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“…A cytoskeletal vortex has not previously been described within any prokaryotes as far as we know. In eukaryotes, a vortex of cytoplasmic motion dependent on microtubules and actin has been shown to be critical for development by driving cytoplasmic streaming in the eggs of several species as well as in plant cells (Schroeder and Battaglia, 1985;Serbus et al, 2005;Stein et al, 2021;Woodhouse and Goldstein, 2013). The eukaryotic cytoskeleton is responsible for the rotation of the nucleus to align with cell polarity in motile cells, particularly fibroblasts (Fruleux and Hawkins, 2016;Gerashchenko et al, 2009;Kim et al, 2014;Levy and Holzbaur, 2008;Maninová et al, 2014;Wu et al, 2011) and has been observed in a vortex-like arrangement during misalignment (Kumar et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli

Birkholz

Laughlin

Suslov

et al. 2021

Preprint

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Vortex-like arrays of cytoskeletal filaments that drive cytoplasmic streaming and nucleus rotation have been identified in eukaryotes, but similar structures have not been described in prokaryotes. The only known example of a rotating intracellular body in prokaryotic cells occurs when nucleus-forming jumbo phages infect Pseudomonas. During infection, a bipolar spindle of PhuZ filaments drives intracellular rotation of the phage nucleus, a key aspect of the replication cycle. Here we show the E. coli jumbo phage Goslar assembles a phage nucleus surrounded by an array of PhuZ filaments resembling a vortex instead of a bipolar spindle. Expression of mutant PhuZ strongly reduces Goslar phage nucleus rotation, demonstrating that the PhuZ cytoskeletal vortex is necessary for rotating the phage nucleus. While vortex-like cytoskeletal arrays are important in eukaryotes, this work identifies the first known example of a coherent assembly of filaments into a vortex-like structure driving intracellular rotation within the prokaryotic cytoplasm.

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Swirling Instability of the Microtubule Cytoskeleton

Cited by 33 publications

References 50 publications

Sustained enzymatic activity and flow in crowded protein droplets

Sustained enzymatic activity and flow in crowded protein droplets

Active nematic order and dynamic lane formation of microtubules driven by membrane-bound diffusing motors

A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli

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