Abstract
Life in complex systems, such as cities and organisms, comes to a standstill when global coordination of mass, energy and information flows is disrupted. Global coordination is no less important in single cells, especially in large oocytes and newly formed embryos, which commonly use fast fluid flows for dynamic reorganization of their cytoplasm. These cytoplasmic streaming flows have been proposed to spontaneously arise from hydrodynamic interactions among cortically anchored microtubules loaded with cargo-carrying molecular motors. Here, we combine modelling and simulation with live imaging to investigate such flows in the Drosophila oocyte. Using a fast, accurate and scalable numerical approach to investigate fluid–structure interactions of thousands of flexible fibres, we demonstrate the robust emergence and evolution of cell-spanning vortices—or twisters—in three-dimensional cellular geometries. These twister flows, dominated by a near-rigid-body rotation with secondary toroidal components, reproduce the variety of experimental observations. In cells, these flows are probably involved in rapid mixing and transport of ooplasmic components.
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Data availability
Simulational and experimental data sets generated during the current study are available from the corresponding author on reasonable request.
Code availability
A publicly available and elaborated version of the SkellySim codebase used to generate the simulations is available at https://github.com/flatironinstitute/SkellySim.
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Acknowledgements
We thank B. Chakraborti, J.I. Alsous, E. Gavis and R. Goldstein for extensive and useful discussions and A. Farhadifar for generously sharing his Blender expertise. We acknowledge support from National Institutes of Health grant nos. R01GM134204 (S.Y.S.) and R35GM131752 (V.I.G.) and National Science Foundation grant no. DMR-2004469 (M.J.S.). Stocks obtained from the Bloomington Drosophila Stock Center, supported by National Institutes of Health grant no. P40OD018537, were used in this study. The computations in this work were performed at facilities supported by the Scientific Computing Core at the Flatiron Institute, a division of the Simons Foundation.
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M.J.S., S.Y.S. and V.I.G. designed the research. S.D., R.F., G.K. and R.B. contributed to simulation software development and simulation data analysis. W.L. and M.L. designed and performed the experiments. S.D., R.F. and M.J.S. developed the image processing software and analysis of experimental data. S.D., R.F., S.Y.S. and M.J.S. prepared the manuscript. All authors contributed to its editing.
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Supplementary Notes 1 and 2 and Figs. 1–9.
Supplementary Video 1
Time course of configurations of microtubules anchored to the interior surface of a sphere in a cut-away view for a simulation with parameters \(\bar{\rho }=5\) and \(\bar{\sigma }=90\) (case I). The timestamp shows time normalized to the relaxation time of a single microtubule.
Supplementary Video 2
Time course of 2D projection of velocity field for a simulation with parameters \(\bar{\rho }=5\) and \(\bar{\sigma }=90\) (case I). The bordering circle represents the boundary of the sphere (case I). The timestamp shows time normalized to the relaxation time of a single microtubule.
Supplementary Video 3
Time course of configurations of microtubules anchored to the interior surface of a sphere in a cut-away view for a simulation with parameters \(\bar{\rho }=15\) and \(\bar{\sigma }=45\) (case II). The timestamp shows time normalized to the relaxation time of a single microtubule.
Supplementary Video 4
Time course of configurations of microtubules anchored to the interior surface of a sphere in a cut-away view for a simulation with parameters \(\bar{\rho }=15\) and \(\bar{\sigma }=45\) (case II). The timestamp shows time normalized to the relaxation time of a single microtubule.
Supplementary Video 5
Live video of a cross-section of a Drosophila oocyte obtained by a brightfield microscope. Scale bar, 50 μm. The timestamp is in units of minutes.
Supplementary Video 6
Time course of the polar order parameter P for a simulation with parameters \(\bar{\rho }=15\) and \(\bar{\sigma }=45\). Left and right views face two diametrically opposite defect-like structures formed in long time. The timestamp shows time normalized to the relaxation time of a single microtubule.
Supplementary Video 7
360∘ rotation of two snapshots at early time (t = 0.025τr, t = 0.035τr) and one snapshot at long time (t = 0.5τr) of a simulation with parameters \(\bar{\rho }=15\) and \(\bar{\sigma }=45\). τr is the relaxation time of a single microtubule. Surface polarity vectors pi corresponding to each microtubule are represented as arrows and superposed on the surface. The colour of the surface represents the polar order parameter P.
Supplementary Video 8
Time course of configurations of microtubules anchored to the interior surface for a cell shape similar to that of an oocyte, shown in two cut-away views. The simulation parameters are \(\bar{\rho }=15\) and \(\bar{\sigma }=45\). The timestamp shows time normalized to the relaxation time of a single microtubule.
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Dutta, S., Farhadifar, R., Lu, W. et al. Self-organized intracellular twisters. Nat. Phys. 20, 666–674 (2024). https://doi.org/10.1038/s41567-023-02372-1
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DOI: https://doi.org/10.1038/s41567-023-02372-1
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