Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Letter
  • Open Access

Synchronization and metachronal waves of elastic cilia caused by unsteady viscous flow

Albert von Kenne1,*, Sonja Schmelter1, Holger Stark2, and Markus Bär1,†

  • *Contact author: a.vonkenne@web.de
  • †Contact author: markus.baer@ptb.de

Phys. Rev. Research 7, L012029 – Published 6 February, 2025

DOI: https://doi.org/10.1103/PhysRevResearch.7.L012029

Abstract

Hydrodynamic coordination of cilia is ubiquitous in biology. It is commonly modeled using the steady Stokes equations. The flow around ciliated cells, however, exhibits finite-time vorticity diffusion, requiring a dynamical description. We present a model of elastic cilia coupled by unsteady viscous flow in the bulk fluid. Therein, vorticity diffusion impacts cilia coordination qualitatively and quantitatively. In particular, pairs of cilia synchronize in antiphase for long diffusion times. Moreover, metachronal waves occur in cilia chains larger than the viscous penetration depth, whereas global synchronization occurs in Stokes flow.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (87)

  1. W. Gilpin, M. S. Bull, and M. Prakash, The multiscale physics of cilia and flagella, Nat. Rev. Phys. 2, 74 (2020).
  2. K. Y. Wan and G. Jékely, On the unity and diversity of cilia, Philos. Trans. R. Soc. London B 375, 20190148 (2020).
  3. M. L. Byron, D. W. Murphy, K. Katija, A. P. Hoover, J. Daniels, K. Garayev, D. Takagi, E. Kanso, B. J. Gemmell, M. Ruszczyk et al., Metachronal motion across scales: Current challenges and future directions, Integr. Comp. Biol. 61, 1674 (2021).
  4. K. Y. Wan and R. N. Poon, Mechanisms and functions of multiciliary coordination, Curr. Opin. Cell Biol. 86, 102286 (2024).
  5. S. L. Tamm, Ciliary motion in paramecium: A scanning electron microscope study, J. Cell Biol. 55, 250 (1972).
  6. 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).
  7. 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).
  8. S. Nonaka, H. Shiratori, Y. Saijoh, and H. Hamada, Determination of left–right patterning of the mouse embryo by artificial nodal flow, Nature (London) 418, 96 (2002).
  9. R. Faubel, C. Westendorf, E. Bodenschatz, and G. Eichele, Cilia-based flow network in the brain ventricles, Science 353, 176 (2016).
  10. O. Mesdjian, C. Wang, S. Gsell, U. Dortona, J. Favier, A. Viallat, and E. Loiseau, Longitudinal to transverse metachronal wave transitions in an in vitro model of ciliated bronchial epithelium, Phys. Rev. Lett. 129, 038101 (2022).
  11. W. Gilpin, V. N. Prakash, and M. Prakash, Vortex arrays and ciliary tangles underlie the feeding–swimming trade-off in starfish larvae, Nat. Phys. 13, 380 (2017).
  12. R. N. Poon, T. A. Westwood, H. Laeverenz-Schlogelhofer, E. Brodrick, J. Craggs, E. E. Keaveny, G. Jékely, and K. Y. Wan, Ciliary propulsion and metachronal coordination in reef coral larvae, Phys. Rev. Res. 5, L042037 (2023).
  13. 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).
  14. E. W. Knight-Jones, Relations between metachronism and the direction of ciliary beat in metazoa, J Cell Sci. 95, 503 (1954).
  15. K. Y. Wan, Coordination of eukaryotic cilia and flagella, Essays Biochem. 62, 829 (2018).
  16. C. Ringers, S. Bialonski, M. Ege, A. Solovev, J. N. Hansen, I. Jeong, B. M. Friedrich, and N. Jurisch-Yaksi, Novel analytical tools reveal that local synchronization of cilia coincides with tissue-scale metachronal waves in zebrafish multiciliated epithelia, eLife 12, e77701 (2023).
  17. X. Dong, G. Z. Lum, W. Hu, R. Zhang, Z. Ren, P. R. Onck, and M. Sitti, Bioinspired cilia arrays with programmable nonreciprocal motion and metachronal coordination, Sci. Adv. 6, eabc9323 (2020).
  18. V. Sahadevan, B. Panigrahi, and C.-Y. Chen, Microfluidic applications of artificial cilia: Recent progress, demonstration, and future perspectives, Micromachines 13, 735 (2022).
  19. T. ul Islam, Y. Wang, I. Aggarwal, Z. Cui, H. E. Amirabadi, H. Garg, R. Kooi, B. B. Venkataramanachar, T. Wang, S. Zhang et al., Microscopic artificial cilia–a review, Lab Chip 22, 1650 (2022).
  20. G. Taylor, Analysis of the swimming of microscopic organisms, Proc. R. Soc. London A 209, 447 (1951).
  21. J. Elgeti and G. Gompper, Emergence of metachronal waves in cilia arrays, Proc. Natl. Acad. Sci. USA 110, 4470 (2013).
  22. D. R. Brumley, K. Y. Wan, M. Polin, and R. E. Goldstein, Flagellar synchronization through direct hydrodynamic interactions, eLife 3, e02750 (2014).
  23. E. Lauga, The Fluid Dynamics of Cell Motility, Vol. 62 (Cambridge University Press, Cambridge, 2020).
  24. E. M. Purcell, Life at low Reynolds number, Am. J. Phys. 45, 3 (1977).
  25. R. Golestanian, J. M. Yeomans, and N. Uchida, Hydrodynamic synchronization at low Reynolds number, Soft Matter 7, 3074 (2011).
  26. J. Elgeti, R. G. Winkler, and G. Gompper, Physics of microswimmers – single particle motion and collective behavior: A review, Rep. Prog. Phys. 78, 056601 (2015).
  27. N. Bruot and P. Cicuta, Realizing the physics of motile cilia synchronization with driven colloids, Annu. Rev. Condens. Matter Phys. 7, 323 (2016).
  28. K. Drescher, R. E. Goldstein, N. Michel, M. Polin, and I. Tuval, Direct measurement of the flow field around swimming microorganisms, Phys. Rev. Lett. 105, 168101 (2010).
  29. S. Gueron, K. Levit-Gurevich, N. Liron, and J. J. Blum, Cilia internal mechanism and metachronal coordination as the result of hydrodynamical coupling, Proc. Natl. Acad. Sci. USA 94, 6001 (1997).
  30. S. Gueron and K. Levit-Gurevich, Energetic considerations of ciliary beating and the advantage of metachronal coordination, Proc. Natl. Acad. Sci. USA 96, 12240 (1999).
  31. M. Cosentino Lagomarsino, B. Bassetti, and P. Jona, Rowers coupled hydrodynamically. modeling possible mechanisms for the cooperation of cilia, Eur. Phys. J. B 26, 81 (2002).
  32. M. Reichert and H. Stark, Synchronization of rotating helices by hydrodynamic interactions, Eur. Phys. J. E 17, 493 (2005).
  33. A. Vilfan and F. Jülicher, Hydrodynamic flow patterns and synchronization of beating cilia, Phys. Rev. Lett. 96, 058102 (2006).
  34. P. Lenz and A. Ryskin, Collective effects in ciliar arrays, Phys. Biol. 3, 285 (2006).
  35. B. Guirao and J.-F. Joanny, Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia, Biophys. J. 92, 1900 (2007).
  36. T. Niedermayer, B. Eckhardt, and P. Lenz, Synchronization, phase locking, and metachronal wave formation in ciliary chains, Chaos 18, 037128 (2008).
  37. N. Uchida and R. Golestanian, Generic conditions for hydrodynamic synchronization, Phys. Rev. Lett. 106, 058104 (2011).
  38. C. Wollin and H. Stark, Metachronal waves in a chain of rowers with hydrodynamic interactions, Eur. Phys. J. E 34, 42 (2011).
  39. N. Osterman and A. Vilfan, Finding the ciliary beating pattern with optimal efficiency, Proc. Natl. Acad. Sci. USA 108, 15727 (2011).
  40. C. Mettot and E. Lauga, Energetics of synchronized states in three-dimensional beating flagella, Phys. Rev. E 84, 061905 (2011).
  41. M. Leoni and T. B. Liverpool, Hydrodynamic synchronization of nonlinear oscillators at low Reynolds number, Phys. Rev. E 85, 040901(R) (2012).
  42. J. Kotar, L. Debono, N. Bruot, S. Box, D. Phillips, S. Simpson, S. Hanna, and P. Cicuta, Optimal hydrodynamic synchronization of colloidal rotors, Phys. Rev. Lett. 111, 228103 (2013).
  43. A. Takamatsu, K. Shinohara, T. Ishikawa, and H. Hamada, Hydrodynamic phase locking in mouse node cilia, Phys. Rev. Lett. 110, 248107 (2013).
  44. B. Nasouri and G. J. Elfring, Hydrodynamic interactions of cilia on a spherical body, Phys. Rev. E 93, 033111 (2016).
  45. D. R. Brumley, N. Bruot, J. Kotar, R. E. Goldstein, P. Cicuta, and M. Polin, Long-range interactions, wobbles, and phase defects in chains of model cilia, Phys. Rev. Fluids 1, 081201 (2016).
  46. R. E. Goldstein, E. Lauga, A. I. Pesci, and M. R. Proctor, Elastohydrodynamic synchronization of adjacent beating flagella, Phys. Rev. Fluids 1, 073201 (2016).
  47. A. Maestro, N. Bruot, J. Kotar, N. Uchida, R. Golestanian, and P. Cicuta, Control of synchronization in models of hydrodynamically coupled motile cilia, Commun. Phys. 1, 28 (2018).
  48. Y. Kawamura and R. Tsubaki, Phase reduction approach to elastohydrodynamic synchronization of beating flagella, Phys. Rev. E 97, 022212 (2018).
  49. K. Okumura, S. Nishikawa, T. Omori, T. Ishikawa, and A. Takamatsu, Asymmetry in cilia configuration induces hydrodynamic phase locking, Phys. Rev. E 97, 032411 (2018).
  50. N. Pellicciotta, E. Hamilton, J. Kotar, M. Faucourt, N. Delgehyr, N. Spassky, and P. Cicuta, Entrainment of mammalian motile cilia in the brain with hydrodynamic forces, Proc. Natl. Acad. Sci. USA 117, 8315 (2020).
  51. E. Hamilton, N. Pellicciotta, L. Feriani, and P. Cicuta, Motile cilia hydrodynamics: Entrainment versus synchronization when coupling through flow, Philos. Trans. R. Soc. London B 375, 20190152 (2020).
  52. F. O. Mannan, M. Jarvela, and K. Leiderman, Minimal model of the hydrodynamical coupling of flagella on a spherical body with application to Volvox, Phys. Rev. E 102, 033114 (2020).
  53. H. Guo, Y. Man, K. Y. Wan, and E. Kanso, Intracellular coupling modulates biflagellar synchrony, J. R. Soc. Interface 18, 20200660 (2021).
  54. I. Tanasijević and E. Lauga, Hydrodynamic synchronization in strong confinement, Phys. Rev. E 103, 022403 (2021).
  55. F. Meng, R. R. Bennett, N. Uchida, and R. Golestanian, Conditions for metachronal coordination in arrays of model cilia, Proc. Natl. Acad. Sci. USA 118, e2102828118 (2021).
  56. W. Liao and E. Lauga, Energetics of synchronization for model flagella and cilia, Phys. Rev. E 103, 042419 (2021).
  57. S. Maretvadakethope, Y. Hwang, and E. E. Keaveny, Synchronized states of hydrodynamically coupled filaments and their stability, Phys. Rev. Fluids 7, 053101 (2022).
  58. A. Solovev and B. M. Friedrich, Synchronization in cilia carpets: Multiple metachronal waves are stable, but one wave dominates, New J. Phys. 24, 013015 (2022).
  59. A. Solovev and B. M. Friedrich, Synchronization in cilia carpets and the Kuramoto model with local coupling: Breakup of global synchronization in the presence of noise, Chaos 32, 013124 (2022).
  60. A. V. Kanale, F. Ling, H. Guo, S. Fürthauer, and E. Kanso, Spontaneous phase coordination and fluid pumping in model ciliary carpets, Proc. Natl. Acad. Sci. USA 119, e2214413119 (2022).
  61. M. Tătulea-Codrean and E. Lauga, Elastohydrodynamic synchronization of rotating bacterial flagella, Phys. Rev. Lett. 128, 208101 (2022).
  62. B. Chakrabarti, S. Fürthauer, and M. J. Shelley, A multiscale biophysical model gives quantized metachronal waves in a lattice of beating cilia, Proc. Natl. Acad. Sci. USA 119, e2113539119 (2022).
  63. D. J. Hickey, R. Golestanian, and A. Vilfan, Nonreciprocal interactions give rise to fast cilium synchronization in finite systems, Proc. Natl. Acad. Sci. USA 120, e2307279120 (2023).
  64. R. R. Bennett, Direction selection of metachronal waves in hydrodynamic coordination of cilia, arXiv:2309.08274.
  65. A. von Kenne, M. Bär, and T. Niedermayer, Hydrodynamic synchronization of elastic cilia: How surface effects determine the characteristics of metachronal waves, Phys. Rev. E 109, 054407 (2024).
  66. B. Friedrich, Hydrodynamic synchronization of flagellar oscillators, Eur. Phys. J.: Spec. Top. 225, 2353 (2016).
  67. G. S. Klindt, C. Ruloff, C. Wagner, and B. M. Friedrich, Load response of the flagellar beat, Phys. Rev. Lett. 117, 258101 (2016).
  68. D. Wei, P. G. Dehnavi, M.-E. Aubin-Tam, and D. Tam, Is the zero Reynolds number approximation valid for ciliary flows? Phys. Rev. Lett. 122, 124502 (2019).
  69. B. Eckhardt and J. Buehrle, Time-dependent effects in high viscosity fluid dynamics, Eur. Phys. J.: Spec. Top. 157, 135 (2008).
  70. D. Wei, P. G. Dehnavi, M.-E. Aubin-Tam, and D. Tam, Measurements of the unsteady flow field around beating cilia, J. Fluid Mech. 915, A70 (2021).
  71. L. D. Landau and E. M. Lifschitz, Hydrodynamik (Akademie Verlag, Berlin, 1991).
  72. N. Bruot, P. Cicuta, H. Bloomfield-Gadêlha, R. E. Goldstein, J. Kotar, E. Lauga, and F. Nadal, Direct measurement of unsteady microscale Stokes flow using optically driven microspheres, Phys. Rev. Fluids 6, 053102 (2021).
  73. M. Theers and R. G. Winkler, Synchronization of rigid microrotors by time-dependent hydrodynamic interactions, Phys. Rev. E 88, 023012 (2013).
  74. C. Brennen, An oscillating-boundary-layer theory for ciliary propulsion, J. Fluid Mech. 65, 799 (1974).
  75. K. C. Leptos, J. S. Guasto, J. P. Gollub, A. I. Pesci, and R. E. Goldstein, Dynamics of enhanced tracer diffusion in suspensions of swimming eukaryotic microorganisms, Phys. Rev. Lett. 103, 198103 (2009).
  76. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevResearch.7.L012029 for a detailed derivation of the model equations and numerical methods omitted from the main text.
  77. A. B. Basset, A Treatise on Hydrodynamics: With Numerous Examples, Vol. 2 (Deighton, Bell and Company, Cambridge, 1888).
  78. J. Boussinesq, Théorie Analytique de la Chaleur: Mise en Harmonie avec la Thermodynamique et avec la Théorie Mécanique de la Lumière, Vol. 2 (Gauthier-Villars, Paris, 1903).
  79. C. W. Oseen, Hydrodynamik (Akademische Verlagsgesellschaft, Leipzig, 1927).
  80. M. R. Maxey and J. J. Riley, Equation of motion for a small rigid sphere in a nonuniform flow, Phys. Fluids 26, 883 (1983).
  81. R. Adler, A study of locking phenomena in oscillators, Proc. IRE 34, 351 (1946).
  82. F. Boselli, J. Jullien, E. Lauga, and R. E. Goldstein, Fluid mechanics of mosaic ciliated tissues, Phys. Rev. Lett. 127, 198102 (2021).
  83. 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).
  84. I. Fouxon and A. Leshansky, Fundamental solution of unsteady Stokes equations and force on an oscillating sphere near a wall, Phys. Rev. E 98, 063108 (2018).
  85. N. Uchida and R. Golestanian, Hydrodynamic synchronization between objects with cyclic rigid trajectories, Eur. Phys. J. E 35, 135 (2012).
  86. 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).
  87. L. Damet, G. M. Cicuta, J. Kotar, M. C. Lagomarsino, and P. Cicuta, Hydrodynamically synchronized states in active colloidal arrays, Soft Matter 8, 8672 (2012).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation