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  • Letter
  • Open Access

Flagellar elasticity and the multiple swimming modes of interfacial bacteria

S. Bianchi1, F. Saglimbeni1, G. Frangipane2,3, and R. Di Leonardo3,1,*

  • 1Soft and Living Matter Laboratory, NANOTEC-CNR, Institute of Nanotechnology, Rome 00185, Italy
  • 2Center for Life Nano and Neuro Science, Italian Institute of Technology, Rome 00161, Italy
  • 3Department of Physics, “Sapienza” University of Rome, Rome 00185, Italy

  • *roberto.dileonardo@uniroma1.it
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Phys. Rev. Research 4, L022044 – Published 24 May, 2022

DOI: https://doi.org/10.1103/PhysRevResearch.4.L022044

Abstract

In peritrichous bacteria, such as E. coli, flagella join into a compact bundle that is usually assumed to be rigidly connected to the cell body allowing only counter-rotations around a common axis. This simple microswimmer model has been very successful in providing quantitative predictions on swimming behavior in bulk fluids and in the proximity of different kinds of interfaces and confinement. Here, we show that, when bacteria colonize a water-air interface, capillary forces can strongly deform the body-bundle complex, giving rise to unusual and heterogeneous swimming modes. We find that all trajectories can be classified into four main modes, with cells tracing either clockwise or counterclockwise circles while the cell body can be locked to the swimming direction or spin freely. All the observed phenomenology can be reproduced by simply allowing elastic bending of the bundle axis, where stiffness is the main factor in selecting the swimming mode. Our results allow us to experimentally test flexible models of microswimmers in highly perturbed contexts and provide physical insights into the early stages of bacterial pellicles.

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References (27)

  1. L. Vaccari, M. Molaei, T. H. Niepa, D. Lee, R. L. Leheny, and K. J. Stebe, Films of bacteria at interfaces, Adv. Colloid Interface Sci. 247, 561 (2017).
  2. J. Deng, M. Molaei, N. G. Chisholm, and K. J. Stebe, Motile bacteria at oil-water interfaces: Pseudomonas aeruginosa, Langmuir 36, 6888 (2020).
  3. D. M. Kaz, R. McGorty, M. Mani, M. P. Brenner, and V. N. Manoharan, Physical ageing of the contact line on colloidal particles at liquid interfaces, Nat. Mater. 11, 138 (2012).
  4. G. Boniello, C. Blanc, D. Fedorenko, M. Medfai, N. B. Mbarek, M. In, M. Gross, A. Stocco, and M. Nobili, Brownian diffusion of a partially wetted colloid, Nat. Mater. 14, 908 (2015).
  5. A. Stocco, B. Chollet, X. Wang, C. Blanc, and M. Nobili, Rotational diffusion of partially wetted colloids at fluid interfaces, J. Colloid Interface Sci. 542, 363 (2019).
  6. K. Dietrich, D. Renggli, M. Zanini, G. Volpe, I. Buttinoni, and L. Isa, Two-dimensional nature of the active Brownian motion of catalytic microswimmers at solid and liquid interfaces, New J. Phys. 19, 065008 (2017).
  7. S. Bianchi, F. Saglimbeni, and R. Di Leonardo, Holographic Imaging Reveals the Mechanism of Wall Entrapment in Swimming Bacteria, Phys. Rev. X 7, 011010 (2017).
  8. E. Lauga, W. R. DiLuzio, G. M. Whitesides, and H. A. Stone, Swimming in circles: Motion of bacteria near solid boundaries, Biophys. J. 90, 400 (2006).
  9. R. Di Leonardo, D. Dell'Arciprete, L. Angelani, and V. Iebba, Swimming with an Image, Phys. Rev. Lett. 106, 038101 (2011).
  10. S. Bianchi, F. Saglimbeni, G. Frangipane, D. Dell'Arciprete, and R. Di Leonardo, 3D dynamics of bacteria wall entrapment at a water–air interface, Soft Matter 15, 3397 (2019).
  11. L. Lemelle, J.-F. Palierne, E. Chatre, and C. Place, Counterclockwise circular motion of bacteria swimming at the air-liquid interface, J. Bacteriol. 192, 6307 (2010).
  12. M. Morse, A. Huang, G. Li, M. R. Maxey, and J. X. Tang, Molecular adsorption steers bacterial swimming at the air/water interface, Biophys. J. 105, 21 (2013).
  13. L. Lemelle, J.-F. Palierne, E. Chatre, C. Vaillant, and C. Place, Curvature reversal of the circular motion of swimming bacteria probes for slip at solid/liquid interfaces, Soft Matter 9, 9759 (2013).
  14. J. Hu, A. Wysocki, R. G. Winkler, and G. Gompper, Physical sensing of surface properties by microswimmers – directing bacterial motion via wall slip, Sci. Rep. 5, 9586 (2015).
  15. J. Higdon, The hydrodynamics of flagellar propulsion: Helical waves, J. Fluid Mech. 94, 331 (1979).
  16. K. Son, J. S. Guasto, and R. Stocker, Bacteria can exploit a flagellar buckling instability to change direction, Nat. Phys. 9, 494 (2013).
  17. H. Shum and E. Gaffney, The effects of flagellar hook compliance on motility of monotrichous bacteria: A modeling study, Phys. Fluids 24, 061901 (2012).
  18. F. Saglimbeni, S. Bianchi, A. Lepore, and R. Di Leonardo, Three-axis digital holographic microscopy for high speed volumetric imaging, Opt. Express 22, 13710 (2014).
  19. S. Bianchi, F. Saglimbeni, A. Lepore, and R. Di Leonardo, Polar features in the flagellar propulsion of E. coli bacteria, Phys. Rev. E 91, 062705 (2015).
  20. S. Ferretti, S. Bianchi, G. Frangipane, and R. Di Leonardo, A virtual reality interface for the immersive manipulation of live microscopic systems, Sci. Rep. 11, 7610 (2021).
  21. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevResearch.4.L022044 for further details on theoretical modeling, simulations, and supporting figures.
  22. S. Kim and S. J. Karrila, Microhydrodynamics: Principles and Selected Applications (Dover, New York, 2005).
  23. ϕ̇=ddttan−1(ly/lx)=lxl̇y−lyl̇xlx2+ly2=(l̂×dl̂/dt)·ẑlx2+ly2. By substituting the time evolution of the orientation versor dl̂dt=ω×l̂ one obtains ϕ̇=(l̂×ω×l̂)·ẑlx2+ly2. Using the triple vector product identity one obtains ϕ̇=(l̂·l̂)(ω·ẑ)−(l̂·ẑ)(l̂·ω)lx2+ly2 that leads to Eq. (10) if the components of l̂ and ω are substituted.
  24. S. W. Reid, M. C. Leake, J. H. Chandler, C.-J. Lo, J. P. Armitage, and R. M. Berry, The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11, Proc. Natl. Acad. Sci. USA 103, 8066 (2006).
  25. N. C. Darnton, L. Turner, S. Rojevsky, and H. C. Berg, On torque and tumbling in swimming Escherichia coli, J. Bacteriol. 189, 1756 (2007).
  26. D. Das and E. Lauga, Computing the motor torque of Escherichia coli, Soft Matter 14, 5955 (2018).
  27. N. C. Darnton and H. C. Berg, Force-extension measurements on bacterial flagella: Triggering polymorphic transformations, Biophys. J. 92, 2230 (2007).

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Phys. Rev. Research 4, L022044– Published 24 May, 2022
  • Received 12 August 2021
  • Revised 16 November 2021
  • Accepted 6 May 2022
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