Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-13T01:43:29.829Z Has data issue: false hasContentIssue false

Hydrodynamics of micro-swimmers in films

Published online by Cambridge University Press:  29 September 2016

A. J. T. M. Mathijssen*
Affiliation:
Rudolf Peierls Centre for Theoretical Physics, University of Oxford, 1 Keble Road, OxfordOX1 3NP, UK
A. Doostmohammadi
Affiliation:
Rudolf Peierls Centre for Theoretical Physics, University of Oxford, 1 Keble Road, OxfordOX1 3NP, UK
J. M. Yeomans
Affiliation:
Rudolf Peierls Centre for Theoretical Physics, University of Oxford, 1 Keble Road, OxfordOX1 3NP, UK
T. N. Shendruk
Affiliation:
Rudolf Peierls Centre for Theoretical Physics, University of Oxford, 1 Keble Road, OxfordOX1 3NP, UK
*
Email address for correspondence: mathijssen@physics.ox.ac.uk

Abstract

One of the principal mechanisms by which surfaces and interfaces affect microbial life is by perturbing the hydrodynamic flows generated by swimming. By summing a recursive series of image systems, we derive a numerically tractable approximation to the three-dimensional flow fields of a stokeslet (point force) within a viscous film between a parallel no-slip surface and a no-shear interface and, from this Green’s function, we compute the flows produced by a force- and torque-free micro-swimmer. We also extend the exact solution of Liron & Mochon (J. Engng Maths, vol. 10 (4), 1976, pp. 287–303) to the film geometry, which demonstrates that the image series gives a satisfactory approximation to the swimmer flow fields if the film is sufficiently thick compared to the swimmer size, and we derive the swimmer flows in the thin-film limit. Concentrating on the thick-film case, we find that the dipole moment induces a bias towards swimmer accumulation at the no-slip wall rather than the water–air interface, but that higher-order multipole moments can oppose this. Based on the analytic predictions, we propose an experimental method to find the multipole coefficient that induces circular swimming trajectories, allowing one to analytically determine the swimmer’s three-dimensional position under a microscope.

Type
Papers
Copyright
© 2016 Cambridge University Press 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ardekani, A. M. & Gore, E. 2012 Emergence of a limit cycle for swimming microorganisms in a vortical flow of a viscoelastic fluid. Phys. Rev. E 85 (5), 056309.CrossRefGoogle Scholar
Bees, M. A., Andresen, P., Mosekilde, E. & Givskov, M. 2000 The interaction of thin-film flow, bacterial swarming and cell differentiation in colonies of Serratia liquefaciens . J. Math. Biol. 40 (1), 2763.Google Scholar
Berg, H. C. & Turner, L. 1990 Chemotaxis of bacteria in glass capillary arrays. Escherichia coli, motility, microchannel plate, and light scattering. Biophys. J. 58 (4), 919930.Google Scholar
Berke, A. P., Turner, L., Berg, H. C. & Lauga, E. 2008 Hydrodynamic attraction of swimming microorganisms by surfaces. Phys. Rev. Lett. 101, 038102.CrossRefGoogle ScholarPubMed
Blake, J. 1971a A spherical envelope approach to ciliary propulsion. J. Fluid Mech. 46 (1), 199208.Google Scholar
Blake, J. R. 1971b A note on the image system for a stokeslet in a no-slip boundary. Proc. Camb. Phil. Soc. 70, 303310.CrossRefGoogle Scholar
Bukoreshtliev, N. V., Haase, K. & Pelling, A. E. 2013 Mechanical cues in cellular signalling and communication. Cell Tissue Res. 352 (1), 7794.CrossRefGoogle ScholarPubMed
Chacón, R. 2013 Chaotic dynamics of a microswimmer in Poiseuille flow. Phys. Rev. E 88 (5), 052905.Google ScholarPubMed
Conrad, J. C. 2012 Physics of bacterial near-surface motility using flagella and type IV pili: implications for biofilm formation. Rev. Microbiol. 163 (9–10), 619629.Google ScholarPubMed
Costanzo, A., Di Leonardo, R., Ruocco, G. & Angelani, L. 2012 Transport of self-propelling bacteria in micro-channel flow. J. Phys.: Condens. Matter 24 (6), 065101.Google Scholar
Crowdy, D., Lee, S., Samson, O., Lauga, E. & Hosoi, A. E. 2011 A two-dimensional model of low-Reynolds number swimming beneath a free surface. J. Fluid Mech. 681, 2447.Google Scholar
Crowdy, D. G. & Or, Y. 2010 Two-dimensional point singularity model of a low-Reynolds-number swimmer near a wall. Phys. Rev. E 81, 036313.Google ScholarPubMed
Dechesne, A., Wang, G., Gülez, G., Or, D. & Smets, B. F. 2010 Hydration-controlled bacterial motility and dispersal on surfaces. Proc. Natl Acad. Sci. USA 107 (32), 1436914372.Google Scholar
Di Leonardo, R., Dell’Arciprete, D., Angelani, L. & Iebba, V. 2011 Swimming with an image. Phys. Rev. Lett. 106, 038101.Google Scholar
Diluzio, W. R., Turner, L., Mayer, M., Garstecki, P., Weibel, D. B., Berg, H. C. & Whitesides, G. M. 2005 Escherichia coli swim on the right-hand side. Nature 435 (7046), 12711274.CrossRefGoogle ScholarPubMed
Doostmohammadi, A., Stocker, R. & Ardekani, A. M. 2012 Low-Reynolds-number swimming at pycnoclines. Proc. Natl Acad. Sci. USA 109 (10), 38563861.Google Scholar
Drescher, K., Leptos, K. C., Tuval, I., Ishikawa, T., Pedley, T. J. & Goldstein, R. E. 2009 Dancing Volvox: hydrodynamic bound states of swimming algae. Phys. Rev. Lett. 102, 168101.CrossRefGoogle ScholarPubMed
Figueroa-Morales, N., Miño, G., Rivera, A., Caballero, R., Clément, E., Altshuler, E. & Lindner, A. 2015 Living on the edge: transfer and traffic of E. coli in a confined flow. Soft Matt. 11, 62846293.CrossRefGoogle Scholar
Frymier, P. D., Ford, R. M., Berg, H. C. & Cummings, P. T. 1995 Three-dimensional tracking of motile bacteria near a solid planar surface. Proc. Natl Acad. Sci. USA 92 (13), 61956199.CrossRefGoogle Scholar
Gachelin, J., Miño, G., Berthet, H., Lindner, A., Rousselet, A. & Clément, É. 2013 Non-Newtonian viscosity of Escherichia coli suspensions. Phys. Rev. Lett. 110 (26), 268103.Google Scholar
Givskov, M., Eberl, L. & Molin, S. 1997 Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens . Fatigue Engng Mater. Struct. Microbiol. Lett. 148 (2), 115122.Google Scholar
de Graaf, J. & Stenhammar, J.2016 Stirring by periodic arrays of microswimmers. Preprint arXiv:1606.00213.CrossRefGoogle Scholar
Grimont, P. A. & Grimont, F. 1978 The genus Serratia . Annu. Rev. Microbiol. 32 (1), 221248.Google Scholar
Guasto, J. S., Johnson, K. A. & Gollub, J. P. 2010 Oscillatory flows induced by microorganisms swimming in two dimensions. Phys. Rev. Lett. 105 (16), 168102.Google ScholarPubMed
Guidobaldi, H. A., Jeyaram, Y., Condat, C. A., Oviedo, M., Berdakin, I., Moshchalkov, V. V., Giojalas, L. C., Silhanek, A. V. & Marconi, V. I. 2015 Disrupting the wall accumulation of human sperm cells by artificial corrugation. Biomicrofluidics 9 (2), 024122.CrossRefGoogle ScholarPubMed
Guzmán-Lastra, F. & Soto, R. 2012 Stochastic resonance on the transverse displacement of swimmers in an oscillatory shear flow. Phys. Rev. E 86, 037301.Google Scholar
Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. 2004 Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2 (2), 95108.CrossRefGoogle ScholarPubMed
Harshey, R. M. 2003 Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 57 (1), 249273.Google Scholar
Harshey, R. M. & Matsuyama, T. 1994 Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc. Natl Acad. Sci. USA 91 (18), 86318635.CrossRefGoogle ScholarPubMed
Hill, J., Kalkanci, O., McMurry, J. L. & Koser, H. 2007 Hydrodynamic surface interactions enable Escherichia coli to seek efficient routes to swim upstream. Phys. Rev. Lett. 98, 068101.Google Scholar
Howse, J. R., Jones, R. A., Ryan, A. J., Gough, T., Vafabakhsh, R. & Golestanian, R. 2007 Self-motile colloidal particles: from directed propulsion to random walk. Phys. Rev. Lett. 99 (4), 048102.Google Scholar
Ishikawa, T., Locsei, J. & Pedley, T. 2010 Fluid particle diffusion in a semidilute suspension of model micro-organisms. Phys. Rev. E 82 (2), 021408.Google Scholar
Ishikawa, T. & Pedley, T. 2007 The rheology of a semi-dilute suspension of swimming model micro-organisms. J. Fluid Mech. 588, 399435.CrossRefGoogle Scholar
Ishimoto, K., Cosson, J. & Gaffney, E. A. 2016 A simulation study of sperm motility hydrodynamics near fish eggs and spheres. J. Theor. Biol. 389, 187197.Google Scholar
Jeanneret, R., Kantsler, V., Pushkin, D. O. & Polin, M. 2016 Entrainment dominates the interaction of microalgae with micron-sized objects. Nat. Commun. 7, 12518.CrossRefGoogle ScholarPubMed
Jepson, A., Martinez, V. A., Schwarz-Linek, J., Morozov, A. & Poon, W. C. 2013 Enhanced diffusion of nonswimmers in a three-dimensional bath of motile bacteria. Phys. Rev. E 88 (4), 041002.Google Scholar
Kantsler, V., Dunkel, J., Blayney, M. & Goldstein, R. E. 2014 Rheotaxis facilitates upstream navigation of mammalian sperm cells. eLife 3, 02403.Google ScholarPubMed
Karimi, A. & Ardekani, A. 2013 Gyrotactic bioconvection at pycnoclines. J. Fluid Mech. 733, 245267.CrossRefGoogle Scholar
Karimi, A., Karig, D., Kumar, A. & Ardekani, A. 2015 Interplay of physical mechanisms and biofilm processes: review of microfluidic methods. Lab on a Chip 15 (1), 2342.Google Scholar
Karimi, A., Yazdi, S. & Ardekani, A. M. 2013 Hydrodynamic mechanisms of cell and particle trapping in microfluidics. Biomicrofluidics 7 (2), 021501.Google Scholar
Katija, K. 2012 Biogenic inputs to ocean mixing. J. Expl Biol. 215 (6), 10401049.Google Scholar
Kim, M. J. & Breuer, K. S. 2007 Controlled mixing in microfluidic systems using bacterial chemotaxis. Anal. Chem. 79 (3), 955959.Google Scholar
Kim, S. & Karilla, S. 1991 Microhydrodynamics: Butterworth Series of Chemical Engineering. Butterworth.Google Scholar
Kurtuldu, H., Guasto, J. S., Johnson, K. A. & Gollub, J. 2011 Enhancement of biomixing by swimming algal cells in two-dimensional films. Proc. Natl Acad. Sci. USA 108 (26), 1039110395.CrossRefGoogle ScholarPubMed
Lambert, R. A., Picano, F., Breugem, W.-P. & Brandt, L. 2013 Active suspensions in thin films: nutrient uptake and swimmer motion. J. Fluid Mech. 733, 528557.Google Scholar
Lauga, E., DiLuzio, W. R., Whitesides, G. M. & Stone, H. A. 2006 Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90 (2), 400412.CrossRefGoogle ScholarPubMed
Lauga, E. & Powers, T. R. 2009 The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72 (9), 096601.Google Scholar
Leptos, K. C., Guasto, J. S., Gollub, J., Pesci, A. I. & Goldstein, R. E. 2009 Dynamics of enhanced tracer diffusion in suspensions of swimming eukaryotic microorganisms. Phys. Rev. Lett. 103 (19), 198103.Google Scholar
Li, G., Bensson, J., Nisimova, L., Munger, D., Mahautmr, P., Tang, J. X., Maxey, M. R. & Brun, Y. V. 2011 Accumulation of swimming bacteria near a solid surface. Phys. Rev. E 84, 041932.Google Scholar
Li, G. & Tang, J. X. 2009 Accumulation of microswimmers near a surface mediated by collision and rotational Brownian motion. Phys. Rev. Lett. 103, 078101.CrossRefGoogle Scholar
Liron, N. & Mochon, S. 1976 Stokes flow for a stokeslet between two parallel flat plates. J. Engng Maths 10 (4), 287303.Google Scholar
Lopez, D. & Lauga, E. 2014 Dynamics of swimming bacteria at complex interfaces. Phys. Fluids 26 (7), 071902.CrossRefGoogle Scholar
López, H. M., Gachelin, J., Douarche, C., Auradou, H. & Clément, E. 2015 Turning bacteria suspensions into superfluids. Phys. Rev. Lett. 115, 028301.CrossRefGoogle ScholarPubMed
Magar, V., Goto, T. & Pedley, T. J. 2003 Nutrient uptake by a self-propelled steady squirmer. Q. J. Mech. Appl. Maths 56 (1), 6591.Google Scholar
Masoud, H. & Stone, H. A. 2014 A reciprocal theorem for Marangoni propulsion. J. Fluid Mech. 741, R4.Google Scholar
Masoud, H., Stone, H. A. & Shelley, M. J. 2013 On the rotation of porous ellipsoids in simple shear flows. J. Fluid Mech. 733, R6.CrossRefGoogle Scholar
Mathijssen, A. J., Pushkin, D. O. & Yeomans, J. M. 2015 Tracer trajectories and displacement due to a micro-swimmer near a surface. J. Fluid Mech. 773, 498519.Google Scholar
Mathijssen, A. J. T. M., Doostmohammadi, A., Yeomans, J. M. & Shendruk, T. N. 2016a Hotspots of boundary accumulation: dynamics and statistics of micro-swimmers in flowing films. J. R. Soc. Interface 13 (115), 20150936.Google Scholar
Mathijssen, A. J. T. M., Shendruk, T. N., Yeomans, J. M. & Doostmohammadi, A. 2016b Upstream swimming in microbiological flows. Phys. Rev. Lett. 116, 028104.Google Scholar
Mino, G., Mallouk, T. E., Darnige, T., Hoyos, M., Dauchet, J., Dunstan, J., Soto, R., Wang, Y., Rousselet, A. & Clement, E. 2011 Enhanced diffusion due to active swimmers at a solid surface. Phys. Rev. Lett. 106 (4), 048102.CrossRefGoogle Scholar
Molaei, M., Barry, M., Stocker, R. & Sheng, J. 2014 Failed escape: solid surfaces prevent tumbling of Escherichia coli . Phys. Rev. Lett. 113 (6), 068103.CrossRefGoogle ScholarPubMed
Or, Y. & Murray, R. M. 2009 Dynamics and stability of a class of low Reynolds number swimmers near a wall. Phys. Rev. E 79, 045302.Google Scholar
Ozarkar, S. S. & Sangani, A. S. 2008 A method for determining Stokes flow around particles near a wall or in a thin film bounded by a wall and a gas–liquid interface. Phys. Fluids 20 (6), 063301.CrossRefGoogle Scholar
Paxton, W. F., Kistler, K. C., Olmeda, C. C., Sen, A., St Angelo, S. K., Cao, Y., Mallouk, T. E., Lammert, P. E. & Crespi, V. H. 2004 Catalytic nanomotors: autonomous movement of striped nanorods. J. Am. Chem. Soc. 126 (41), 1342413431.CrossRefGoogle ScholarPubMed
Pedley, T. J. & Kessler, J. O. 1987 The orientation of spheroidal microorganisms swimming in a flow field. Proc. R. Soc. Lond. B 231 (1262), 4770.Google Scholar
Pushkin, D. O. & Yeomans, J. M. 2014 Stirring by swimmers in confined microenvironments. J. Stat. Mech. 2014 (4), P04030.Google Scholar
Quiñones, B., Dulla, G. & Lindow, S. E. 2005 Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae . Mol. Plant–Microbe Interact. 18 (7), 682693.Google Scholar
Spagnolie, S. E. & Lauga, E. 2012 Hydrodynamics of self-propulsion near a boundary: predictions and accuracy of far-field approximations. J. Fluid Mech. 700, 105147.Google Scholar
Staben, M. E., Zinchenko, A. Z. & Davis, R. H. 2003 Motion of a particle between two parallel plane walls in low-Reynolds-number Poiseuille flow. Phys. Fluids 15 (6), 17111733.Google Scholar
Stone, H. A. & Masoud, H. 2015 Mobility of membrane-trapped particles. J. Fluid Mech. 781, 494505.Google Scholar
Vaccari, L., Allan, D., Sharifi-Mood, N., Singh, A., Leheny, R. & Stebe, K. 2015 Films of bacteria at interfaces: three stages of behaviour. Soft Matt. 11, 60626074.Google Scholar
Valadares, L. F., Tao, Y.-G., Zacharia, N. S., Kitaev, V., Galembeck, F., Kapral, R. & Ozin, G. A. 2010 Catalytic nanomotors: self-propelled sphere dimers. Small 6 (4), 565572.Google Scholar
Wang, S. & Ardekani, A. M. 2013 Swimming of a model ciliate near an air–liquid interface. Phys. Rev. E 87, 063010.Google Scholar
Zöttl, A. & Stark, H. 2012 Nonlinear dynamics of a microswimmer in Poiseuille flow. Phys. Rev. Lett. 108 (21), 218104.Google Scholar
Zöttl, A. & Stark, H. 2013 Periodic and quasiperiodic motion of an elongated microswimmer in Poiseuille flow. Eur. Phys. J. E 36 (1), 4.Google Scholar