PreprintCited by 2Microtubule and mitosis dynamicsMicro and Nano RoboticsCellular Mechanics and Interactions

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Chiral and nematic phases of flexible active filaments

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Dunajova, Zuzana, Mateu, Batirtze Prats, Radler, Philipp, Lim, Keesiang, Velicky, Philipp, Danzl, Johann Georg, Wong, Richard W., Elgeti, Jens, Hannezo, Edouard, Loose, Martin·2022·bioRxiv (Cold Spring Harbor Laboratory)

Preprint — published as 10.1038/s41567-023-02218-w · Paper page

Abstract

The emergence of large-scale order in self-organized systems relies on local interactions between individual components. During bacterial cell division, the tubulin-homolog FtsZ polymerizes into treadmilling filaments that further assemble into a cytoskeletal ring. Although minimal in vitro assays have shown the striking self-organization capacity of FtsZ filaments, such as dynamic chiral assemblies, how these large-scale structures emerge and relate to individual filament properties remains poorly understood. To understand this quantitatively, we combined minimal chiral active matter simulations with biochemical reconstitution experiments. Using STED and TIRF microscopy as well as high-speed AFM, we imaged the behavior of FtsZ filaments on different spatial scales. Simulations and experiments revealed that filament density and flexibility define the local and global order of the system: At intermediate densities, flexible filaments organize into chiral rings and polar bands, while an effectively nematic organization dominates for high filament densities and for mutant filaments with increased rigidity. Our predicted phase diagram captured these features quantitatively, demonstrating how filament flexibility, density and chirality cooperate with activity to give rise to a large repertoire of collective behaviors. These properties are likely important for the dynamic organization of soft chiral matter, including that of treadmilling FtsZ filaments during bacterial cell division.

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Research works printed but not linked: 62

  1. 10.1126/science.aao5434 · DOI
  2. 10.1103/PhysRevLett.116.178301 · DOI
  3. 10.1073/pnas.2017047118 · DOI
  4. 2022, Activity-induced polar patterns of filaments gliding on a sphere, Nature Communications, 13, 2579, 10.1038/s41467-022-30128-7 · DOI
  5. 10.1038/nature10874 · DOI
  6. 2020, Computational models for active matter, Nat Rev Phys, 2, 181, 10.1038/s42254-020-0152-1 · DOI
  7. 2020, The 2020 motile active matter roadmap, J. Phys.: Condens. Matter, 32, 193001
  8. 2010, Polar patterns of driven filaments, 467, 73
  9. 2010, Control of actin filament treadmilling in cell motility, Annual review of biophysics, 39, 449, 10.1146/annurev-biophys-051309-103849 · DOI
  10. 2020, Physical Models of Collective Cell Migration, Annu. Rev. Condens. Matter Phys, 11, 77, 10.1146/annurev-conmatphys-031218-013516 · DOI
  11. Reymann, A.-C. , Staniscia, F. , Erzberger, A. , Salbreux, G. & Grill, S. W. Cortical flow aligns actin filaments to form a furrow. eLife 5, (2016). · DOI
  12. 2022, Active nematics across scales from cytoskeleton organization to tissue morphogenesis, Current Opinion in Genetics & Development, 73, 101897, 10.1016/j.gde.2021.101897 · DOI
  13. 10.1016/j.cell.2019.05.052 · DOI
  14. 10.1103/RevModPhys.85.1143 · DOI
  15. 10.1088/1361-6633/aab6bb) · DOI
  16. 2022, Symmetry, Thermodynamics, and Topology in Active Matter, Phys. Rev. X, 12, 010501
  17. 10.1140/epje/i2012-12089-6 · DOI
  18. 10.1209/0295-5075/ac8f69 · DOI
  19. 2022, Topological active matter, Nat Rev Phys, 4, 380, 10.1038/s42254-022-00445-3 · DOI
  20. 2020, Insights into the Structure, Function, and Dynamics of the Bacterial Cytokinetic FtsZ-Ring, Annual Review of Biophysics, 49, 309, 10.1146/annurev-biophys-121219-081703 · DOI
  21. 10.1007/s00239-003-2523-5 · DOI
  22. Wagstaff, J. M. et al. A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments. mBio 8, (2017). · DOI
  23. 2021, FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation in Bacillus subtilis cell division, Nature Communications, 12, 2448, 10.1038/s41467-021-22526-0 · DOI
  24. 10.1016/j.cub.2019.12.023 · DOI
  25. 10.1016/j.cub.2004.06.048 · DOI
  26. 10.1073/pnas.0807963106 · DOI
  27. 10.1073/pnas.1514296113 · DOI
  28. 10.1038/ncb2885 · DOI · Paper page
  29. 2018, Collective dynamics of self-propelled semiflexible filaments, Soft Matter, 14, 4483, 10.1039/C8SM00282G · DOI
  30. 2020, Collective motion of driven semiflexible filaments tuned by soft repulsion and stiffness, Soft Matter, 16, 9436, 10.1039/D0SM01036G · DOI
  31. 2015, Self-propelled worm-like filaments: spontaneous spiral formation, structure, and dynamics, Soft Matter, 11, 7181, 10.1039/C5SM01683E · DOI
  32. 10.7554/eLife.35578 · DOI
  33. 10.1371/journal.pone.0012682 · DOI
  34. 10.1038/s41467-019-13702-4 · DOI
  35. 2020, Chapter 8 Computational analysis of filament polymerization dynamics in cytoskeletal networks, 158, 145
  36. 10.1073/pnas.211400898 · DOI
  37. 10.1016/j.cbpa.2019.05.010 · DOI
  38. Haeusser, D. P. , Rowlett, V. W. & Margolin, W. A mutation in Escherichia coli ftsZ bypasses the requirement for the essential division gene zipA and confers resistance to FtsZ assembly inhibitors by stabilizing protofilament bundling. Mol Microbiol 97, 988–1005. · DOI
  39. 2017, Escherichia coli FtsA forms lipid-bound minirings that antagonize lateral interactions between FtsZ protofilaments, Nature communications, 8, 15957, 10.1038/ncomms15957 · DOI
  40. 2022, ColabFold: making protein folding accessible to all, Nature methods, 19, 679, 10.1038/s41592-022-01488-1 · DOI · Paper page
  41. 10.1021/ja303564a · DOI
  42. 10.7554/eLife.32471 · DOI
  43. 2022, Bacterial divisome protein FtsA forms curved antiparallel double filaments when binding to FtsN, Nat Microbiol, 7, 1686, 10.1038/s41564-022-01206-9 · DOI
  44. 2020, Chiral-filament self-assembly on curved manifolds, Soft Matter, 16, 10548, 10.1039/D0SM01339K · DOI
  45. 2022, Collective migration reveals mechanical flexibility of malaria parasites, Nature Physics, 18, 586, 10.1038/s41567-022-01583-2 · DOI
  46. 2022, Odd dynamics of living chiral crystals, Nature, 607, 287, 10.1038/s41586-022-04889-6 · DOI
  47. 2018, Spontaneous shear flow in confined cellular nematics, Nature Physics, 14, 728, 10.1038/s41567-018-0099-7 · DOI
  48. 2017, Chirality in microbial biofilms is mediated by close interactions between the cell surface and the substratum, ISME J, 11, 1688, 10.1038/ismej.2017.19 · DOI
  49. 10.1038/ncb3137 · DOI
  50. 10.1126/science.aak9995 · DOI
  51. 10.1126/science.aak9973 · DOI
  52. 2022, In vitro reconstitution of Escherichia coli divisome activation, Nat Commun, 13, 2635, 10.1038/s41467-022-30301-y · DOI
  53. 2020, High-Speed AFM Reveals Molecular Dynamics of Human Influenza A Hemagglutinin and Its Interaction with Exosomes, Nano Lett, 20, 6320, 10.1021/acs.nanolett.0c01755 · DOI
  54. 2021, Millisecond dynamic of SARS-CoV-2 spike and its interaction with ACE2 receptor and small extracellular vesicles, J Extracell Vesicles, 10, e12170, 10.1002/jev2.12170 · DOI
  55. 2022, Spatiotemporal tracking of small extracellular vesicle nanotopology in response to physicochemical stresses revealed by HS-AFM, J Extracell Vesicles, 11, e12275, 10.1002/jev2.12275 · DOI
  56. 10.1073/pnas.0604965103 · DOI
  57. Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nature Methods Preprint at https://doi.org/10.1038/nmeth.2019 (2012). · DOI · Paper page
  58. 10.1021/ma502264c · DOI
  59. 10.1016/j.commatsci.2019.109363 · DOI
  60. 2022, Measurement of the persistence length of cytoskeletal filaments using curvature distributions, Biophysical Journal, 121, 1813, 10.1016/j.bpj.2022.04.020 · DOI
  61. 2020, freud: A software suite for high throughput analysis of particle simulation data, Computer Physics Communications, 254, 107275, 10.1016/j.cpc.2020.107275 · DOI
  62. 10.1101/2021.10.04.463034 · DOI · Paper page

Metadata

Authors
Dunajova, Z., Mateu, B. P., Radler, P., Lim, K., Velicky, P., Danzl, J. G., Wong, R. W., Elgeti, J., Hannezo, E., & Loose, M.
Affiliations
  • Institute of Science and Technology Austria (AT)
  • Kanazawa University (JP)
  • Forschungszentrum Jülich (DE)
Corresponding author
Loose, Martin
Venue
bioRxiv (Cold Spring Harbor Laboratory)
Publisher
openRxiv
Published
2022-12-16
OpenAlex
W4313310808
Cited by
2
References
1
Citations by year
2023: 2
Type
posted content
Language
en
Open access
Licence
cc-by
Locations
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Institute of Science and Technology Austria (submittedVersion, cc-by)
Funders
  • Institute of Science and Technology Austria
  • Kanazawa University
  • Österreichischen Akademie der Wissenschaften
  • Austrian Science Fund (P34607)
  • H2020 European Research Council (679239)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Physical Sciences › Physics and Astronomy › Condensed Matter Physics › Micro and Nano Robotics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Keywords
active matter, nematic order, filament flexibility, bacterial cell division, chiral ring, phase diagram, filament density, chiral active matter

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