Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T15:19:37.099Z Has data issue: false hasContentIssue false

A three-dimensional model of flagellar swimming in a Brinkman fluid

Published online by Cambridge University Press:  14 February 2019

NguyenHo Ho
Affiliation:
Department of Mathematics, Bridgewater State University, 131 Summer Street, Bridgewater, MA 02325, USA
Karin Leiderman
Affiliation:
Applied Mathematics and Statistics, Colorado School of Mines, 1500 Illinois Street, Golden, CO 80401, USA
Sarah Olson*
Affiliation:
Department of Mathematical Sciences, Worcester Polytechnic Institute, 100 Institute Road, Worcester, MA 01609, USA
*
Email address for correspondence: [email protected]

Abstract

We investigate three-dimensional flagellar swimming in a fluid with a sparse network of stationary obstacles or fibres. The Brinkman equation is used to model the average fluid flow where a flow-dependent term, including a resistance parameter that is inversely proportional to the permeability, captures the effects of the fibres on the fluid. To solve for the local linear and angular velocities that are coupled to the flagellar motion, we extend the method of regularized Brinkmanlets to incorporate a Kirchhoff rod, discretized as point forces and torques along a centreline. Representing a flagellum as a Kirchhoff rod, we investigate emergent waveforms for different preferred strain and twist functions. Since the Kirchhoff rod formulation allows for out-of-plane motion, in addition to studying a preferred planar sine wave configuration, we also study a preferred helical configuration. Our numerical method is validated by comparing results to asymptotic swimming speeds derived for an infinite-length cylinder propagating planar or helical waves. Similar to the asymptotic analysis for both planar and helical bending, we observe that with small amplitude bending, swimming speed is always enhanced relative to the case with no fibres in the fluid (Stokes) as the resistance parameter is increased. For regimes not accounted for with asymptotic analysis, i.e. large amplitude planar and helical bending, our model results show a non-monotonic change in swimming speed with respect to the resistance parameter; a maximum swimming speed is observed when the resistance parameter is near one. The non-monotonic behaviour is due to the emergent waveforms; as the resistance parameter increases, the swimmer becomes incapable of achieving the amplitude of its preferred configuration. We also show how simulation results of slower swimming speeds for larger resistance parameters are actually consistent with the asymptotic swimming speeds if work in the system is fixed.

Type
JFM Papers
Copyright
© 2019 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

Ahmadi, E., Cortez, R. & Fujioka, H. 2017 Boundary integral formulation for flows containing an interface between two porous media. J. Fluid Mech. 816, 7193.10.1017/jfm.2017.42Google Scholar
Auriault, J. L. 2009 On the domain of validity of Brinkman’s equation. Trans. Porous Med. 79, 215223.10.1007/s11242-008-9308-7Google Scholar
Babcock, D. F., Wandernoth, P. M. & Wennemuth, G. 2014 Episodic rolling and transient attachments create diversity in sperm swimming behavior. BMC Biol. 12 (67), 112.10.1186/s12915-014-0067-3Google Scholar
Brinkman, H. C. 1947 A calculation of the viscous force exerted by a flowing fluid on a dense swarm of paticles. Appl. Sci. Res. A1, 2734.Google Scholar
Chouaieb, N. & Maddocks, J. H. 2004 Kirchhoff’s problem of helical equilibria of uniform rods. J. Elast. 77 (3), 221247.10.1007/s10659-005-0931-zGoogle Scholar
Cortez, R. 2001 The method of regularized Stokeslets. SIAM J. Sci. Comput. 23, 12041225.Google Scholar
Cortez, R., Cummins, B., Leiderman, K. & Varela, D. 2010 Computation of three-dimensional Brinkman flows using regularized methods. J. Comput. Phys. 229, 76097624.10.1016/j.jcp.2010.06.012Google Scholar
Cortez, R., Fauci, L. & Medovikov, A. 2005 The method of regularized Stokeslets in three dimensions: Analysis, validation, and application to helical swimming. Phys. Fluids 17, 12041224.10.1063/1.1830486Google Scholar
Crisfield, M. A. 1997 Non-Linear Finite Element Analysis of Solids and Structures: Advanced Topics, 1st edn. Wiley.Google Scholar
Dineen, S. 1998 Multivariate Calculus and Geometry, 3rd edn. Springer.Google Scholar
Djuričković, B., Goriely, A. & Maddocks, J. H. 2013 Twist and stretch of helices explained via the Kirchhoff-Love rod model of elastic filaments. Phys. Rev. Lett. 111 (10), 108103.Google Scholar
Durlofsky, L. & Brady, J. F. 1987 Analysis of the Brinkman equation as a model for flow in porous media. Phys. Fluids 30 (11), 33293341.Google Scholar
Elgeti, J., Kaupp, U. B. & Gompper, G. 2010 Hydrodynamics of sperm cells near surfaces. Biophys. J. 99 (4), 10181026.10.1016/j.bpj.2010.05.015Google Scholar
Fauci, L. & Dillon, R. 2006 Biofluidmechanics of reproduction. Annu. Rev. Fluid Mech. 38, 371394.10.1146/annurev.fluid.37.061903.175725Google Scholar
Fauci, L. & McDonald, A. 1995 Sperm motility in the presence of boundaries. Bull. Math. Biol. 57, 679699.Google Scholar
Feng, J., Ganatos, P. & Weinbaum, S. 1998 Motion of a sphere near planar confining boundaries in a Brinkman medium. J. Fluid Mech. 375, 265296.Google Scholar
Fu, H., Shenoy, V. B. & Powers, T. R. 2010 Low Reynolds number swimming in gels. Europhys. Lett. 91.10.1209/0295-5075/91/24002Google Scholar
Fu, H., Wolgemuth, C. W. & Powers, T. R. 2009 Swimming speeds of filaments in nonlinearly viscoelastic fluids. Phys. Fluids 21, 033102.Google Scholar
Gaffney, E. A., Gadêlha, H., Smith, D. J., Blake, J. R. & Kirkman-Brown, J. C. 2011 Mammalian sperm motility: observation and theory. Annu. Rev. Fluid Mech. 43, 501528.10.1146/annurev-fluid-121108-145442Google Scholar
Goriely, A. & Tabor, M. 1997 Nonlinear dynamics of filaments. III. Instabilities of helical rods. Proc. R. Soc. Lond. A 453, 25832601.Google Scholar
Ho, H. C. & Suarez, S. S. 2001 Hyperactivation of mammalian spermatozoa: function and regulation. Reprod. 122, 519526.10.1530/rep.0.1220519Google Scholar
Ho, N., Olson, S. D. & Leiderman, K. 2016 Swimming speeds of filaments in viscous fluids with resistance. Phys. Rev. E 93 (4), 043108.Google Scholar
Howells, I. D. 1974 Drag due to the motion of a Newtonian fluid through a sparse random array of small fixed rigid objects. J. Fluid Mech. 64, 449475.10.1017/S0022112074002503Google Scholar
Jung, S. 2010 Caenorhabditis elegans swimming in a saturated particulate system. Phys. Fluids 22, 031903.10.1063/1.3359611Google Scholar
Katz, D. F. & Berger, S. A. 1980 Flagellar propulsion of human sperm in cervical mucus. Biorheol. 17, 169175.10.3233/BIR-1980-171-218Google Scholar
Katz, D. F., Drobnis, E. Z. & Overstreet, J. W. 1989 Factors regulating mammalian sperm migration through the female reproductive tract and oocyte vestments. Gamete Res. 22, 443469.10.1002/mrd.1120220410Google Scholar
Lai, S. K., Wang, Y. Y., Hida, K., Crone, R. & Hanes, J. 2009 Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses. Proc. Natl Acad. Sci. USA 107, 598603.Google Scholar
Lauga, E. 2007 Propulsion in a viscoelastic fluid. Phys. Fluids 19, 083104.10.1063/1.2751388Google Scholar
Lee, W., Kim, Y., Olson, S. D. & Lim, S. 2014 Nonlinear dynamics of a rotating elastic rod in a viscous fluid. Phys. Rev. E 90, 033012.Google Scholar
Leiderman, K. & Olson, S. D. 2016 Swimming in a two-dimensional Brinkman fluid: computational modeling and regularized solutions. Phys. Fluids 28 (2), 021902.10.1063/1.4941258Google Scholar
Leshansky, A. M. 2009 Enhanced low-Reynolds-number propulsion in heterogeneous viscous environments. Phys. Rev. E 80, 051911.Google Scholar
Lesich, K., Pelle, D. & Lindemann, C. 2008 Insights into the mechanism of ADP action of flagellar motility derived from studies of bull sperm. Biophys. J. 95, 472482.10.1529/biophysj.107.127951Google Scholar
Lim, S. 2010 Dynamics of an open elastic rod with intrinsic curvature and twist in a viscous fluid. Phys. Fluids 22, 20662083.10.1063/1.3326075Google Scholar
Lim, S., Ferent, A., Wang, S. X. & Peskin, C. S. 2008 Dynamics of a closed rod with twist and bend in fluid. SIAM J. Sci. Comput. 31, 273302.10.1137/070699780Google Scholar
Lim, S. & Peskin, C. 2004 Simulations of the whirling instability by the immersed boundary method. SIAM J. Sci. Comput. 25 (26), 20662083.Google Scholar
Lindemann, C. B. & Lesich, K. A. 2010 Flagellar and ciliary beating: the proven and the possible. J. Cell Sci. 123 (4), 519528.10.1242/jcs.051326Google Scholar
Loewenberg, M. 1993 The unsteady Stokes resistance of arbitrarily oriented, finite-length cylinders. Phys. Fluids A 5, 30043006.10.1063/1.858707Google Scholar
Loewenberg, M. 1994 Axisymmetric unsteady Stokes flow past an oscillating finite-length cylinder. J. Fluid Mech. 265, 265288.10.1017/S0022112094000832Google Scholar
Mattner, P. E. 1968 The distribution of spermatozoa and leucocytes in the female genital tract in goats and cattle. J. Reprod. Fertil. 17, 253261.Google Scholar
Miki, K. 2007 Energy metabolism and sperm function. Soc. Reprod. Fertility Suppl. 65, 309325.Google Scholar
Miki, K. & Clapham, D. E. 2013 Rheotaxis guides mammalian sperm. Curr. Biol. 23, 443452.10.1016/j.cub.2013.02.007Google Scholar
Miradbagheri, S. A. & Fu, H. C. 2016 Helicobacter pylori couples motility and diffusion to actively create a heterogeneous complex medium in gastric diseases. Phys. Rev. Lett. 116, 198101.Google Scholar
Montenegro-Johnson, T. D., Smith, A. A., Smith, D. J., Loghin, D. & Blake, J. R. 2012 Modelling the fluid mechanics of cilia and flagella in reproduction and development. Eur. Phys. J. E 35, 111118.10.1140/epje/i2012-12111-1Google Scholar
Morandotti, M. 2012 Self-propelled micro-swimmers in a Brinkman fluid. J. Biol. Dyn. 6, 88103.10.1080/17513758.2011.611260Google Scholar
Nganguia, H. & Pak, O. S. 2018 Squirming motion in a Brinkman medium. J. Fluid Mech. 855, 554573.10.1017/jfm.2018.685Google Scholar
Nguyen, H. N. & Cortez, R. 2014 Reduction of the regularization error of the method of regularized Stokeslets for a rigid object immersed in a three-dimensional stokes flow. Commun. Comput. Phys. 15 (1), 126152.10.4208/cicp.021112.290413aGoogle Scholar
Nguyen, H. N., Olson, S. D. & Leiderman, K. 2016 A fast method to compute triply-periodic Brinkman flows. Comput. Fluids 133 (15), 5567.10.1016/j.compfluid.2016.04.007Google Scholar
Olson, S. D. 2014 Motion of filaments with planar and helical bending waves in a viscous fluid. In Biological Fluid Dynamics: Modeling, Computation, and Applications (ed. Layton, A. & Olson, S.), A.M.S. Contemp. Math. Series, pp. 109128. AMS.Google Scholar
Olson, S. D. & Fauci, L. 2015 Hydrodynamic interactions of sheets versus filaments: attraction, synchronization, and alignment. Phys. Fluids 27, 121901.10.1063/1.4936967Google Scholar
Olson, S. D. & Leiderman, K. 2015 Effect of fluid resistance on symmetric and asymmetric flagellar waveforms. J. Aero. Aqua. Bio-mech. 4, 1217.10.5226/jabmech.4.12Google Scholar
Olson, S. D., Lim, S. & Cortez, R. 2013 Modeling the dynamics of an elastic rod with intrinsic curvature and twist using a regularized Stokes formulation. J. Comput. Phys. 238, 169187.Google Scholar
Olson, S. D., Suarez, S. S. & Fauci, L. 2011a Coupling biochemistry and hydrodynamics captures hyperactivated sperm motility in a simple flagellar model. J. Theor. Biol. 283, 203216.10.1016/j.jtbi.2011.05.036Google Scholar
Olson, S. D., Suarez, S. S. & Fauci, L. 2011b Coupling biochemistry and hydrodynamics captures hyperactivated sperm motility in a simple flagellar model. J. Theor. Biol. 283 (1), 203216.Google Scholar
Pelle, D. W., Brokaw, C. J., Lesich, K. A. & Lindemann, C. B. 2009 Mechanical properties of the passive sea urchin sperm flagellum. Cell Motil. Cytoskel. 66 (9), 721735.10.1002/cm.20401Google Scholar
Pozrikidis, C. 1989a A singularity method for unsteady linearized flow. Phys. Fluids A 1, 15081520.Google Scholar
Pozrikidis, C. 1989b A study of linearized oscillatory flow past particles by the boundary-integral method. J. Fluid Mech. 202, 1741.10.1017/S0022112089001084Google Scholar
Rutllant, J., Lopez-Bejar, M. & Lopez-Gatius, F. 2001 Confocal scanning laser microscopy examination of bovine vaginal fluid at oestrus. Anat. Histol. Embryol. 30, 159162.10.1111/j.1439-0264.2001.t01-1-0275.xGoogle Scholar
Rutllant, J., Lopez-Bejar, M. & Lopez-Gatius, F. 2005 Ultrastructural and rheological properties of bovine vaginal fluid and its relation to sperm motility and fertilization: a review. Reprod. Dom. Anim. 40, 7986.10.1111/j.1439-0531.2004.00510.xGoogle Scholar
Saltzman, W. M., Radomsky, M. L., Whaley, K. J. & Cone, R. A. 1994 Antibody diffusion in human cervical mucus. Biophys. J. 66, 508515.Google Scholar
Schmitz-Lesich, K. A. & Lindemann, C. B. 2004 Direct measurement of the passive stiffness of rat sperm and implications to the mechanism of the calcium response. Cell Motil. Cytoskel. 59, 169179.Google Scholar
Smith, D. J., Gaffney, E. A., Blake, J. R. & Kirkman-Brown, J. C. 2009a Human sperm accumulation near surfaces: a simulation study. J. Fluid Mech. 621, 289320.10.1017/S0022112008004953Google Scholar
Smith, D. J., Gaffney, E. A., Gadelha, H., Kapur, N. & Kirkman-Brown, J. C. 2009b Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. Cell Motil. Cytoskel. 66, 220236.10.1002/cm.20345Google Scholar
Spielman, L. & Goren, S. L. 1968 Model for predicting pressure drop and filtration efficiency in fibrous media. Environ. Sci. Technol. 1 (4), 279287.Google Scholar
Suarez, S. S. 2010 How do sperm get to the egg? Bioengineering expertise needed! Exp. Mech. 50, 12671274.10.1007/s11340-009-9312-zGoogle Scholar
Suarez, S. S. & Dai, X. 1992 Hyperactivation enhances mouse sperm capacity for penetrating viscoelastic media. Biol. Reprod. 46, 686691.10.1095/biolreprod46.4.686Google Scholar
Suarez, S. S. & Pacey, A. A. 2006 Sperm transport in the female reproductive tract. Human Reprod. Update 12, 2337.10.1093/humupd/dmi047Google Scholar
Taylor, G. I. 1952 The action of waving cylindrical tails in propelling microscopic organisms. Proc. R. Soc. Lond. A 211, 225239.Google Scholar
Taylor, G. I. 1951 Analysis of the swimming of microscopic organisms. Proc. R. Soc. Lond. A 209, 447461.Google Scholar
Teran, J., Fauci, L. & Shelley, M. 2010 Viscoelastic fluid response can increase the speed of a free swimmer. Phys. Rev. Lett. 104, 038101-4.Google Scholar
Thomases, B. & Guy, R. D. 2014 Mechanisms of elastic enhancement and hindrance for finite-length undulatory swimmers in viscoelastic fluids. Phys. Rev. Lett. 113, 098102.10.1103/PhysRevLett.113.098102Google Scholar
Vernon, G. G. & Woolley, D. M. 1999 Three-dimensional motion of avian spermatozoa. Cell Motil. Cytoskel. 42 (2), 149161.10.1002/(SICI)1097-0169(1999)42:2<149::AID-CM6>3.0.CO;2-03.0.CO;2-0>Google Scholar
Woolley, D. M. & Vernon, G. G. 2001 A study of helical and planar waves on sea urchin sperm flagella, with a theory of how they are generated. J. Expl Biol. 204, 13331345.Google Scholar