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Synchronized states of hydrodynamically coupled filaments and their stability

Smitha Maretvadakethope*

Yongyun Hwang

Eric E. Keaveny

  • Department of Mathematical Sciences, University of Liverpool, Mathematical Sciences Building, Liverpool L69 7ZL, United Kingdom

  • Department of Aeronautics, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom

  • Department of Mathematics, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom

  • *sm6412@liverpool.ac.uk
  • y.hwang@imperial.ac.uk
  • e.keaveny@imperial.ac.uk

Phys. Rev. Fluids 7, 053101 – Published 5 May, 2022

DOI: https://doi.org/10.1103/PhysRevFluids.7.053101

Abstract

Cilia and flagella are organelles that play central roles in unicellular locomotion, embryonic development, and fluid transport around tissues. In these examples, multiple cilia are often found in close proximity and exhibit coordinated motion. Inspired by the flagellar motion of biflagellate cells, we examine the synchrony exhibited by a filament pair surrounded by a viscous fluid and tethered to a rigid planar surface. A geometrically switching base moment drives filament motion, and we characterize how the stability of synchonized states depends on the base torque magnitude. In particular, we study the emergence of bistability that occurs when the antiphase, breast-stroke branch becomes unstable. Using a bisection algorithm, we find the unstable edge state that exists between the two basins of attraction when the system exhibits bistability. We establish a bifurcation diagram, study the nature of the bifurcation points, and find that the observed dynamical system can be captured by a modified version of Adler's equation. The bifurcation diagram and presence of bistability reveal a simple mechanism by which the antiphase breast stroke can be modulated, or switched entirely to in-phase undulations through the variation of a single bifurcation parameter.

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References (51)

  1. I. Gibbons, Cilia and flagella of eukaryotes, J. Cell Biol. 91, 107s (1981).
  2. E. A. Gaffney, H. Gadêlha, D. Smith, J. Blake, and J. Kirkman-Brown, Mammalian sperm motility: Observation and theory, Annu. Rev. Fluid Mech. 43, 501 (2011).
  3. R. E. Goldstein, Green algae as model organisms for biological fluid dynamics, Annu. Rev. Fluid Mech. 47, 343 (2015).
  4. C. Brennen and H. Winet, Fluid mechanics of propulsion by cilia and flagella, Annu. Rev. Fluid Mech. 9, 339 (1977).
  5. D. J. Smith, T. D. Montenegro-Johnson, and S. S. Lopes, Symmetry-breaking cilia-driven flow in embryogenesis, Annu. Rev. Fluid Mech. 51, 105 (2019).
  6. M. A. Sleigh, J. R. Blake, and N. Liron, The propulsion of mucus by cilia, Am. Rev. Respir. Dis. 137, 726 (1988).
  7. R. Faubel, C. Westendorf, E. Bodenschatz, and G. Eichele, Cilia-based flow network in the brain ventricles, Science 353, 176 (2016).
  8. E. M. Purcell, Life at low Reynolds number, Physics and Our World: Reissue of the Proceedings of a Symposium in Honor of Victor F Weisskopf (World Scientific, Singapore, 2014), pp. 47–67.
  9. U. Rüffer and W. Nultsch, High-speed cinematographic analysis of the movement of chlamydomonas, Cell Motil. 5, 251 (1985).
  10. R. E. Goldstein, M. Polin, and I. Tuval, Noise and Synchronization in Pairs of Beating Eukaryotic Flagella, Phys. Rev. Lett. 103, 168103 (2009).
  11. M. Polin, I. Tuval, K. Drescher, J. P. Gollub, and R. E. Goldstein, Chlamydomonas swims with two gears in a eukaryotic version of run-and-tumble locomotion, Science 325, 487 (2009).
  12. K. Fujiu, Y. Nakayama, A. Yanagisawa, M. Sokabe, and K. Yoshimura, ChlamydomonasCAV2 encodes a voltage-dependent calcium channel required for the flagellar waveform conversion, Curr. Biol. 19, 133 (2009).
  13. K. Y. Wan and R. E. Goldstein, Time Irreversibility and Criticality in the Motility of a Flagellate Microorganism, Phys. Rev. Lett. 121, 058103 (2018).
  14. K. Y. Wan, Coordination of eukaryotic cilia and flagella, Essays Biochem. 62, 829 (2018).
  15. D. R. Brumley, K. Y. Wan, M. Polin, and R. E. Goldstein, Flagellar synchronization through direct hydrodynamic interactions, eLife 3, e02750 (2014).
  16. G. Quaranta, M.-E. Aubin-Tam, and D. Tam, Hydrodynamics versus Intracellular Coupling in the Synchronization of Eukaryotic Flagella, Phys. Rev. Lett. 115, 238101 (2015).
  17. K. Y. Wan and R. E. Goldstein, Coordinated beating of algal flagella is mediated by basal coupling, Proc. Natl. Acad. Sci. USA 113, E2784 (2016).
  18. V. F. Geyer, F. Jülicher, J. Howard, and B. M. Friedrich, Cell-body rocking is a dominant mechanism for flagellar synchronization in a swimming alga, Proc. Natl. Acad. Sci. USA 110, 18058 (2013).
  19. D. Mondal, R. Adhikari, and P. Sharma, Internal friction controls active ciliary oscillations near the instability threshold, Sci. Adv. 6, eabb0503 (2020).
  20. D. B. Hill, V. Swaminathan, A. Estes, J. Cribb, E. T. O'Brien, C. W. Davis, and R. Superfine, Force generation and dynamics of individual cilia under external loading, Biophys. J. 98, 57 (2010).
  21. J. Elgeti and G. Gompper, Emergence of metachronal waves in cilia arrays, Proc. Natl. Acad. Sci. USA 110, 4470 (2013).
  22. J. Han and C. S. Peskin, Spontaneous oscillation and fluid–structure interaction of cilia, Proc. Natl. Acad. Sci. USA 115, 4417 (2018).
  23. R. Golestanian, J. M. Yeomans, and N. Uchida, Hydrodynamic synchronization at low Reynolds number, Soft Matter 7, 3074 (2011).
  24. D. R. Brumley, M. Polin, T. J. Pedley, and R. E. Goldstein, Hydrodynamic Synchronization and Metachronal Waves on the Surface of the Colonial Alga Volvox carteri, Phys. Rev. Lett. 109, 268102 (2012).
  25. D. R. Brumley, M. Polin, T. J. Pedley, and R. E. Goldstein, Metachronal waves in the flagellar beating of volvox and their hydrodynamic origin, J. R. Soc., Interface 12, 20141358 (2015).
  26. N. Bruot and P. Cicuta, Realizing the physics of motile cilia synchronization with driven colloids, Annu. Rev. Condens. Matter Phys. 7, 323 (2016).
  27. P. Lenz and A. Ryskin, Collective effects in ciliar arrays, Phys. Biol. 3, 285 (2006).
  28. T. Niedermayer, B. Eckhardt, and P. Lenz, Synchronization, phase locking, and metachronal wave formation in ciliary chains, Chaos 18, 037128 (2008).
  29. R. Adler, A study of locking phenomena in oscillators, Proc. IRE 34, 351 (1946).
  30. N. Uchida and R. Golestanian, Hydrodynamic synchronization between objects with cyclic rigid trajectories, Eur. Phys. J. E 35, 135 (2012).
  31. J. Kotar, M. Leoni, B. Bassetti, M. C. Lagomarsino, and P. Cicuta, Hydrodynamic synchronization of colloidal oscillators, Proc. Natl. Acad. Sci. USA 107, 7669 (2010).
  32. G. S. Klindt, C. Ruloff, C. Wagner, and B. M. Friedrich, Load Response of the Flagellar Beat, Phys. Rev. Lett. 117, 258101 (2016).
  33. N. Uchida and R. Golestanian, Synchronization and Collective Dynamics in a Carpet of Microfluidic Rotors, Phys. Rev. Lett. 104, 178103 (2010).
  34. G. S. Klindt, C. Ruloff, C. Wagner, and B. M. Friedrich, In-phase and anti-phase flagellar synchronization by waveform compliance and basal coupling, New J. Phys. 19, 113052 (2017).
  35. Y. Liu, R. Claydon, M. Polin, and D. R. Brumley, Transitions in synchronization states of model cilia through basal-connection coupling, J. R. Soc., Interface 15, 20180450 (2018).
  36. H. Guo, L. Fauci, M. Shelley, and E. Kanso, Bistability in the synchronization of actuated microfilaments, J. Fluid Mech. 836, 304 (2018).
  37. K. C. Leptos, K. Y. Wan, M. Polin, I. Tuval, A. I. Pesci, and R. E. Goldstein, Antiphase Synchronization in a Flagellar-Dominance Mutant of Chlamydomonas, Phys. Rev. Lett. 111, 158101 (2013).
  38. S. F. Schoeller, A. K. Townsend, T. A. Westwood, and E. E. Keaveny, Methods for suspensions of passive and active filaments, J. Comput. Phys. 424, 109846 (2021).
  39. J. W. Swan and J. F. Brady, Simulation of hydrodynamically interacting particles near a no-slip boundary, Phys. Fluids 19, 113306 (2007).
  40. E. E. Keaveny and M. J. Shelley, Applying a second-kind boundary integral equation for surface tractions in Stokes flow, J. Comput. Phys. 230, 2141 (2011).
  41. J. D. Skufca, J. A. Yorke, and B. Eckhardt, Edge of Chaos in a Parallel Shear Flow, Phys. Rev. Lett. 96, 174101 (2006).
  42. Y. Man and E. Kanso, Multisynchrony in Active Microfilaments, Phys. Rev. Lett. 125, 148101 (2020).
  43. G. De Canio, E. Lauga, and R. E. Goldstein, Spontaneous oscillations of elastic filaments induced by molecular motors, J. R. Soc., Interface 14, 20170491 (2017).
  44. F. Ling, H. Guo, and E. Kanso, Instability-driven oscillations of elastic microfilaments, J. R. Soc., Interface 15, 20180594 (2018).
  45. H. Guo, Y. Man, K. Y. Wan, and E. Kanso, Intracellular coupling modulates biflagellar synchrony, J. R. Soc., Interface 18, 20200660 (2021).
  46. E.-M. Holland, F.-J. Braun, C. Nonnengässer, H. Harz, and P. Hegemann, The nature of rhodopsin-triggered photocurrents in Chlamydomonas. I. Kinetics and influence of divalent ions, Biophys. J. 70, 924 (1996).
  47. G. L. Wheeler, Calcium-dependent signalling processes in Chlamydomonas, Chlamydomonas: Molecular Genetics and Physiology (Springer, New York, 2017), pp. 233–255.
  48. A. Babataheri, M. Roper, M. Fermigier, and O. Du Roure, Tethered fleximags as artificial cilia, J. Fluid Mech. 678, 5 (2011).
  49. Y. Wang, Y. Gao, H. Wyss, P. Anderson, and J. den Toonder, Out of the cleanroom, self-assembled magnetic artificial cilia, Lab Chip 13, 3360 (2013).
  50. H. Gu, Q. Boehler, H. Cui, E. Secchi, G. Savorana, C. De Marco, S. Gervasoni, Q. Peyron, T.-Y. Huang, S. Pane et al., Magnetic cilia carpets with programmable metachronal waves, Nat. Commun. 11, 1 (2020).
  51. H. Zhang, L. Koens, E. Lauga, A. Mourran, and M. Möller, A light-driven microgel rotor, Small 15, 1903379 (2019).

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