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Active Fréedericksz Transition in Active Nematic Droplets

Salman Alam1, Bibi Najma1, Abhinav Singh2,3,4, Jeremy Laprade1, Gauri Gajeshwar1, Hannah G. Yevick1, Aparna Baskaran1, Peter J. Foster1,†, and Guillaume Duclos1,*

  • *Contact author: gduclos@brandeis.edu
  • †Present address: Department of Physics and Astronomy, Bridge Institute, Michelson Center for Convergent Bioscience, University of Southern California, Los Angeles, California 90089, USA.

Phys. Rev. X 14, 041002 – Published 3 October, 2024

DOI: https://doi.org/10.1103/PhysRevX.14.041002

Abstract

Active nematic liquid crystals have the remarkable ability to spontaneously deform and flow in the absence of any external driving force. While living materials with orientational order, such as the mitotic spindle, can self-assemble in quiescent active phases, reconstituted active systems often display chaotic, periodic, or circulating flows under confinement. Quiescent in vitro active nematics are, therefore, quite rare, despite the prediction from active hydrodynamic theory that confinement between two parallel plates can suppress flows. This spontaneous flow transition—named the active Fréedericksz transition by analogy with the conventional Fréedericksz transition in passive nematic liquid crystals under a magnetic field—has been a cornerstone of the field of active matter. Here, we report experimental evidence that confinement in spherical droplets can stabilize the otherwise chaotic dynamics of a 3D extensile active nematics, giving rise to a quiescent—yet still out-of-equilibrium—nematic liquid crystal. The active nematics spontaneously flow when confined in larger droplets. The composite nature of our model system composed of extensile bundles of microtubules and molecular motors dispersed in a passive colloidal liquid crystal allows us to demonstrate how the interplay of activity, nematic elasticity, and confinement impacts the spontaneous flow transition. The critical diameter increases when motor concentration decreases or nematic elasticity increases. Experiments and simulations also demonstrate that the critical confinement depends on the confining geometry, with the critical diameter in droplets being larger than the critical width in channels. Biochemical assays reveal that neither confinement nor nematic elasticity impacts the energy-consumption rate, confirming that the quiescent active phase is the stable out-of-equilibrium phase predicted theoretically. Further experiments in dense arrays of monodisperse droplets show that fluctuations in the droplet composition can smooth the flow transition close to the critical diameter. In conclusion, our work provides experimental validation of the active Fréedericksz transition in 3D active nematics, with potential applications in human health, ecology, and soft robotics.

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References (96)

  1. A. Doostmohammadi, J. Ignes-Mullol, J. M. Yeomans, and F. Sagues, Active nematics, Nat. Commun. 9, 3246 (2018).
  2. S. Shankar, A. Souslov, M. J. Bowick, M. C. Marchetti, and V. Vitelli, Topological active matter, Nat. Rev. Phys. 4, 380 (2022).
  3. M. J. Bowick, N. Fakhri, M. C. Marchetti, and S. Ramaswamy, Symmetry, thermodynamics, and topology in active matter, Phys. Rev. X 12, 010501 (2022).
  4. V. Narayan, S. Ramaswamy, and N. Menon, Long-lived giant number fluctuations in a swarming granular nematic, Science 317, 105 (2007).
  5. K. Kawaguchi, R. Kageyama, and M. Sano, Topological defects control collective dynamics in neural progenitor cell cultures, Nature (London) 545, 327 (2017).
  6. T. B. Saw, A. Doostmohammadi, V. Nier, L. Kocgozlu, S. Thampi, Y. Toyama, P. Marcq, C. T. Lim, J. M. Yeomans, and B. Ladoux, Topological defects in epithelia govern cell death and extrusion, Nature (London) 544, 212 (2017).
  7. G. Duclos, S. Garcia, H. G. Yevick, and P. Silberzan, Perfect nematic order in confined monolayers of spindle-shaped cells, Soft Matter 10, 2346 (2014).
  8. J. Nijjer, M. Kothari, C. Li, T. Henzel, Q. Zhang, J. B. Tai, S. Zhou, S. Zhang, T. Cohen, and J. Yan, Biofilms as self-shaping growing nematics, Nat. Phys. 19, 1936 (2023).
  9. Y. I. Yaman, E. Demir, R. Vetter, and A. Kocabas, Emergence of active nematics in chaining bacterial biofilms, Nat. Commun. 10, 2285 (2019).
  10. R. Hartmann, P. K. Singh, P. Pearce, R. Mok, B. Song, F. Diaz-Pascual, J. Dunkel, and K. Drescher, Emergence of three-dimensional order and structure in growing biofilms, Nat. Phys. 15, 251 (2019).
  11. K. Copenhagen, R. Alert, N. S. Wingreen, and J. W. Shaevitz, Topological defects promote layer formation in myxococcus xanthus colonies, Nat. Phys. 17, 211 (2020).
  12. J. Brugues and D. Needleman, Physical basis of spindle self-organization, Proc. Natl. Acad. Sci. U.S.A. 111, 18496 (2014).
  13. R. A. Simha and S. Ramaswamy, Hydrodynamic fluctuations and instabilities in ordered suspensions of self-propelled particles, Phys. Rev. Lett. 89, 058101 (2002).
  14. R. Voituriez, J.-F. Joanny, and J. Prost, Spontaneous flow transition in active polar gels, Europhys. Lett. 70, 404 (2005).
  15. G. Duclos, C. Blanch-Mercader, V. Yashunsky, G. Salbreux, J. F. Joanny, J. Prost, and P. Silberzan, Spontaneous shear flow in confined cellular nematics, Nat. Phys. 14, 728 (2018).
  16. P. Chandrakar, M. Varghese, S. A. Aghvami, A. Baskaran, Z. Dogic, and G. Duclos, Confinement controls the bend instability of three-dimensional active liquid crystals, Phys. Rev. Lett. 125, 257801 (2020).
  17. S. Ramaswamy and M. Rao, Active-filament hydrodynamics: Instabilities, boundary conditions and rheology, New J. Phys. 9, 423 (2007).
  18. T. Sanchez, D. T. Chen, S. J. DeCamp, M. Heymann, and Z. Dogic, Spontaneous motion in hierarchically assembled active matter, Nature (London) 491, 431 (2012).
  19. A. Singh, Q. Vagne, F. Jülicher, and I. F. Sbalzarini, Spontaneous flow instabilities of active polar fluids in three dimensions, Phys. Rev. Res. 5, L022061 (2023).
  20. V. Fréedericksz and A. Repiewa, Theoretisches und experimentelles zur frage nach der natur der anisotropen flüssigkeiten, Z. Phys. 42, 532 (1927).
  21. V. Fréedericksz and V. Zolina, Forces causing the orientation of an anisotropic liquid, Trans. Faraday Soc. 29, 919 (1933).
  22. K.-T. Wu, J. B. Hishamunda, D. T. Chen, S. J. DeCamp, Y.-W. Chang, A. Fernández-Nieves, S. Fraden, and Z. Dogic, Transition from turbulent to coherent flows in confined three-dimensional active fluids, Science 355, eaal1979 (2017).
  23. H. Wioland, F. G. Woodhouse, J. Dunkel, J. O. Kessler, and R. E. Goldstein, Confinement stabilizes a bacterial suspension into a spiral vortex, Phys. Rev. Lett. 110, 268102 (2013).
  24. E. Lushi, H. Wioland, and R. E. Goldstein, Fluid flows created by swimming bacteria drive self-organization in confined suspensions, Proc. Natl. Acad. Sci. U.S.A. 111, 9733 (2014).
  25. M. Ravnik and J. M. Yeomans, Confined active nematic flow in cylindrical capillaries, Phys. Rev. Lett. 110, 026001 (2013).
  26. M. Varghese, A. Baskaran, M. F. Hagan, and A. Baskaran, Confinement-induced self-pumping in 3D active fluids, Phys. Rev. Lett. 125, 268003 (2020).
  27. S. Chandragiri, A. Doostmohammadi, J. M. Yeomans, and S. P. Thampi, Flow states and transitions of an active nematic in a three-dimensional channel, Phys. Rev. Lett. 125, 148002 (2020).
  28. A. Opathalage, M. M. Norton, M. P. Juniper, B. Langeslay, S. A. Aghvami, S. Fraden, and Z. Dogic, Self-organized dynamics and the transition to turbulence of confined active nematics, Proc. Natl. Acad. Sci. U.S.A. 116, 4788 (2019).
  29. J. Hardoüin, R. Hughes, A. Doostmohammadi, J. Laurent, T. Lopez-Leon, J. M. Yeomans, J. Ignés-Mullol, and F. Sagués, Reconfigurable flows and defect landscape of confined active nematics, Commun. Phys. 2, 121 (2019).
  30. T. N. Shendruk, A. Doostmohammadi, K. Thijssen, and J. M. Yeomans, Dancing disclinations in confined active nematics, Soft Matter 13, 3853 (2017).
  31. A. Mozaffari, R. Zhang, N. Atzin, and J. J. de Pablo, Defect spirograph: Dynamical behavior of defects in spatially patterned active nematics, Phys. Rev. Lett. 126, 227801 (2021).
  32. C. G. Wagner, M. M. Norton, J. S. Park, and P. Grover, Exact coherent structures and phase space geometry of preturbulent 2D active nematic channel flow, Phys. Rev. Lett. 128, 028003 (2022).
  33. F. Mori, S. Bhattacharyya, J. M. Yeomans, and S. P. Thampi, Viscoelastic confinement induces periodic flow reversals in active nematics, Phys. Rev. E 108, 064611 (2023).
  34. S. J. DeCamp, G. S. Redner, A. Baskaran, M. F. Hagan, and Z. Dogic, Orientational order of motile defects in active nematics, Nat. Mater. 14, 1110 (2015).
  35. N. Kumar, R. Zhang, J. J. d. Pablo, and M. L. Gardel, Tunable structure and dynamics of active liquid crystals, Sci. Adv. 4, eaat7779 (2018).
  36. A. J. Tan, E. Roberts, S. A. Smith, U. A. Olvera, J. Arteaga, S. Fortini, K. A. Mitchell, and L. S. Hirst, Topological chaos in active nematics, Nat. Phys. 15, 1033 (2019).
  37. L. M. Lemma, S. J. DeCamp, Z. You, L. Giomi, and Z. Dogic, Statistical properties of autonomous flows in 2D active nematics, Soft Matter 15, 3264 (2019).
  38. L. M. Lemma, M. Varghese, T. D. Ross, M. Thomson, A. Baskaran, and Z. Dogic, Spatiotemporal patterning of extensile active stresses in microtubule-based active fluids, Proc. Natl. Acad. Sci. U.S.A. 2, pgad130 (2023).
  39. P. Guillamat, J. Ignes-Mullol, and F. Sagues, Taming active turbulence with patterned soft interfaces, Nat. Commun. 8, 564 (2017).
  40. B. Martínez-Prat, R. Alert, F. Meng, J. Ignés-Mullol, J.-F. Joanny, J. Casademunt, R. Golestanian, and F. Sagués, Scaling regimes of active turbulence with external dissipation, Phys. Rev. X 11, 031065 (2021).
  41. B. Lemma, L. M. Lemma, S. C. Ems-McClung, C. E. Walczak, Z. Dogic, and D. J. Needleman, Structure and dynamics of motor-driven microtubule bundles, Soft Matter 20, 5715 (2024).
  42. G. Duclos, R. Adkins, D. Banerjee, M. S. E. Peterson, M. Varghese, I. Kolvin, A. Baskaran, R. A. Pelcovits, T. R. Powers, A. Baskaran, F. Toschi, M. F. Hagan, S. J. Streichan, V. Vitelli, D. A. Beller, and Z. Dogic, Topological structure and dynamics of three-dimensional active nematics, Science 367, 1120 (2020).
  43. Z. Dogic and S. Fraden, Cholesteric phase in virus suspensions, Langmuir 16, 7820 (2000).
  44. P. Bieling, I. A. Telley, and T. Surrey, A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps, Cell 142, 420 (2010).
  45. R. Subramanian, E. M. Wilson-Kubalek, C. P. Arthur, M. J. Bick, E. A. Campbell, S. A. Darst, R. A. Milligan, and T. M. Kapoor, Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein, Cell 142, 433 (2010).
  46. P. Chandrakar, J. Berezney, B. Lemma, B. Hishamunda, A. Berry, K. T. Wu, R. Subramanian, J. Chung, D. Needleman, J. Gelles, and Z. Dogic, Engineering stability, longevity, and miscibility of microtubule-based active fluids, Soft Matter 18, 1825 (2022).
  47. J. Berezney, B. L. Goode, S. Fraden, and Z. Dogic, Extensile to contractile transition in active microtubule-actin composites generates layered asters with programmable lifetimes, Proc. Natl. Acad. Sci. U.S.A. 119, e2115895119 (2022).
  48. R. Adkins, I. Kolvin, Z. You, S. Witthaus, M. C. Marchetti, and Z. Dogic, Dynamics of active liquid interfaces, Science 377, 768 (2022).
  49. B. Najma, M. Varghese, L. Tsidilkovski, L. Lemma, A. Baskaran, and G. Duclos, Competing instabilities reveal how to rationally design and control active crosslinked gels, Nat. Commun. 13, 6465 (2022).
  50. S. A. Redford, J. Colen, J. L. Shivers, S. Zemsky, M. Molaei, C. Floyd, P. V. Ruijgrok, V. Vitelli, Z. Bryant, A. R. Dinner, and M. L. Gardel, Motor crosslinking augments elasticity in active nematics, Soft Matter 20, 2480 (2024).
  51. D. A. Gagnon, C. Dessi, J. P. Berezney, R. Boros, Daniel T.-N. Chen, Z. Dogic, and D. L. Blair, Shear-induced gelation of self-yielding active networks, Phys. Rev. Lett. 125, 178003 (2020).
  52. K. Visscher, M. J. Schnitzer, and S. M. Block, Single kinesin molecules studied with a molecular force clamp, Nature (London) 400, 184 (1999).
  53. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevX.14.041002 for Supplemental Videos.
  54. L. Giomi, Geometry and topology of turbulence in active nematics, Phys. Rev. X 5, 031003 (2015).
  55. S. L. Anna, N. Bontoux, and H. A. Stone, Formation of dispersions using “flow focusing” in microchannels, Appl. Phys. Lett. 82, 364 (2003).
  56. A. Singh, P. Incardona, and I. F. Sbalzarini, A c++ expression system for partial differential equations enables generic simulations of biological hydrodynamics, Eur. Phys. J. E 44, 117 (2021).
  57. D. D. Hackney and W. Jiang, Assays for kinesin microtubule-stimulated AT pase activity, Methods Mol. Biol. 164, 65 (2001).
  58. D. T. Chen, M. Heymann, S. Fraden, D. Nicastro, and Z. Dogic, ATP consumption of eukaryotic flagella measured at a single-cell level, Biophys. J. 109, 2562 (2015).
  59. L. Radnai, R. F. Stremel, J. R. Sellers, G. Rumbaugh, and C. A. Miller, A semi-high-throughput adaptation of the NADH-coupled atpase assay for screening small molecule inhibitors, J. Vis. Exp 150, e60017 (2019).
  60. B. Najma, W.-S. Wei, A. Baskaran, P. J. Foster, and G. Duclos, Microscopic interactions control a structural transition in active mixtures of microtubules and molecular motors, Proc. Natl. Acad. Sci. U.S.A. 121, e2300174121 (2024).
  61. B. Martínez-Prat, J. Ignés-Mullol, J. Casademunt, and F. Sagués, Selection mechanism at the onset of active turbulence, Nat. Phys. 15, 362 (2019).
  62. G. Duclos, C. Erlenkämper, J.-F. Joanny, and P. Silberzan, Topological defects in confined populations of spindle-shaped cells, Nat. Phys. 13, 58 (2016).
  63. C. Blanch-Mercader, V. Yashunsky, S. Garcia, G. Duclos, L. Giomi, and P. Silberzan, Turbulent dynamics of epithelial cell cultures, Phys. Rev. Lett. 120, 208101 (2018).
  64. S. Čopar, J. Aplinc, Žiga Kos, S. Žumer, and M. Ravnik, Topology of three-dimensional active nematic turbulence confined to droplets, Phys. Rev. X 9, 031051 (2019).
  65. L. J. Ruske and J. M. Yeomans, Morphology of active deformable 3D droplets, Phys. Rev. X 11, 021001 (2021).
  66. Kos and J. Dunkel, Nematic bits and universal logic gates, Sci. Adv. 8, eabp8371 (2022).
  67. T. H. Tan, J. Liu, P. W. Miller, M. Tekant, J. Dunkel, and N. Fakhri, Topological turbulence in the membrane of a living cell, Nat. Phys. 16, 657 (2020).
  68. J. Liu, J. F. Totz, P. W. Miller, A. D. Hastewell, Y.-C. Chao, J. Dunkel, and N. Fakhri, Topological braiding and virtual particles on the cell membrane, Proc. Natl. Acad. Sci. U.S.A. 118, e2104191118 (2021).
  69. S. Zhou, A. Sokolov, O. D. Lavrentovich, and I. S. Aranson, Living liquid crystals, Proc. Natl. Acad. Sci. U.S.A. 111, 1265 (2014).
  70. M. M. Genkin, A. Sokolov, O. D. Lavrentovich, and I. S. Aranson, Topological defects in a living nematic ensnare swimming bacteria, Phys. Rev. X 7, 011029 (2017).
  71. P. C. Mushenheim, R. R. Trivedi, H. H. Tuson, D. B. Weibel, and N. L. Abbott, Dynamic self-assembly of motile bacteria in liquid crystals, Soft Matter 10, 88 (2014).
  72. P. J. Foster, J. Bae, B. Lemma, J. Zheng, W. Ireland, P. Chandrakar, R. Boros, Z. Dogic, D. J. Needleman, and J. J. Vlassak, Dissipation and energy propagation across scales in an active cytoskeletal material, Proc. Natl. Acad. Sci. U.S.A. 120, e2207662120 (2023).
  73. E. Arunachalam, W. Ireland, X. Yang, and D. Needleman, Dissecting flux balances to measure energetic costs in cell biology: Techniques and challenges, Annu. Rev. Condens. Matter Phys. 14, 211 (2023).
  74. J. Li, J. M. Horowitz, T. R. Gingrich, and N. Fakhri, Quantifying dissipation using fluctuating currents, Nat. Commun. 10, 1666 (2019).
  75. C. Battle, C. P. Broedersz, N. Fakhri, V. F. Geyer, J. Howard, C. F. Schmidt, and F. C. MacKintosh, Broken detailed balance at mesoscopic scales in active biological systems, Science 352, 604 (2016).
  76. T. H. Tan, G. A. Watson, Y.-C. Chao, J. Li, T. R. Gingrich, J. M. Horowitz, and N. Fakhri, Scale-dependent irreversibility in living matter, arXiv:2107.05701.
  77. D. S. Seara, B. B. Machta, and M. P. Murrell, Irreversibility in dynamical phases and transitions, Nat. Commun. 12, 392 (2021).
  78. C. E. Fernandez Noa, P. E. Harunari, M. J. de Oliveira, and C. E. Fiore, Entropy production as a tool for characterizing nonequilibrium phase transitions, Phys. Rev. E 100, 012104 (2019).
  79. T. Tomé and M. J. de Oliveira, Entropy production in nonequilibrium systems at stationary states, Phys. Rev. Lett. 108, 020601 (2012).
  80. S. B. Nicholson, L. P. García-Pintos, A. del Campo, and J. R. Green, Time–information uncertainty relations in thermodynamics, Nat. Phys. 16, 1211 (2020).
  81. Y. Hara and A. Kimura, An allometric relationship between mitotic spindle width, spindle length, and ploidy in caenorhabditis elegans embryos, Mol. Biol. Cell 24, 1411 (2013).
  82. C. P. Kelleher, Y. Rana, and D. J. Needleman, Long-range repulsion between chromosomes in mammalian oocyte spindles, arXiv:2211.00883v3.
  83. E. M. Rieckhoff, F. Berndt, M. Elsner, S. Golfier, F. Decker, K. Ishihara, and J. Brugués, Spindle scaling is governed by cell boundary regulation of microtubule nucleation, Curr. Biol. 30, 4973.
  84. M. Castoldi and A. V. Popov, Purification of brain tubulin through two cycles of polymerization–depolymerization in a high-molarity buffer, Protein expression and purification 32, 83 (2003).
  85. A. Hyman, D. Drechsel, D. Kellogg, S. Salser, K. Sawin, P. Steffen, L. Wordeman, and T. Mitchison, Preparation of modified tubulins, in Molecular Motors and the Cytoskeleton, Methods in Enzymology Vol. 196 (Academic Press, New York, 1991), Chap. 39, pp. 478–485.
  86. D. S. Martin, R. Fathi, T. J. Mitchison, and J. Gelles, FRET measurements of kinesin neck orientation reveal a structural basis for processivity and asymmetry, Proc. Natl. Acad. Sci. U.S.A. 107, 5453 (2010).
  87. E. C. Young, H. K. Mahtani, and J. Gelles, One-headed kinesin derivatives move by a nonprocessive, low-duty ratio mechanism unlike that of two-headed kinesin, Biochemistry 37, 3467 (1998).
  88. E. Grelet and S. Fraden, What is the origin of chirality in the cholesteric phase of virus suspensions?, Phys. Rev. Lett. 90, 198302 (2003).
  89. A. M. Tayar, L. M. Lemma, and Z. Dogic, Assembling microtubule-based active matter active matter, in Microtubules: Methods and Protocols (Springer, New York, 2022), pp. 1511–83, 10.1007/978-1-0716-1983-4_10.
  90. B. Renault, R. Ragot, N. Lesevre, and A. Remond, Onset and offset of brain events as indices of mental chronometry, Science 215, 1413 (1982).
  91. A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, Advanced methods of microscope control using μ manager software, J. Biol. Methods 1, e10 (2014), https://polscientific.com/journal/JBM/1/2/10.14440/jbm.2014.36.
  92. W. Thielicke and R. Sonntag, Particle image velocimetry for matlab: Accuracy and enhanced algorithms in PIVlab, J. Open Res. Software 9, 12 (2021).
  93. A. Singh, P. H. Suhrcke, P. Incardona, and I. F. Sbalzarini, A numerical solver for active hydrodynamics in three dimensions and its application to active turbulence, Phys. Fluids 35, 105155 (2023).
  94. P. Incardona, A. Leo, and Y. Zaluzhnyi, OpenFPM: A scalable open framework for particle and particle-mesh codes on parallel computers, Comput. Phys. Commun. 241, 155 (2019).
  95. B. Schrader, S. Reboux, and I. F. Sbalzarini, Discretization correction of general integral PSE operators for particle methods, J. Comput. Phys. 229, 4159 (2010).
  96. S. Balay, W. D. Gropp, L. C. McInnes, and B. F. Smith, Efficient management of parallelism in object-oriented numerical software libraries, in Modern Software Tools for Scientific Computing, edited by E. Arge, A. M. Bruaset, and H. P. Langtangen (Birkhäuser, Boston, 1997), pp. 163–202.

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