Synchronization and bundling of anchored bacterial flagella

The synchronization and bundling process of bacterial flagella is investigated by mesoscale hydrodynamic simulations. Systems with two to six flagella are considered, which are anchored at one end, and are driven by a constant torque. A flagellum is modelled as a linear helical structure composed of mass points with their elastic shape maintained by bonds, bending, and torsional potentials. The characteristic times for synchronization and bundling are analyzed in terms of motor torque, separation, and number of flagella. We find that hydrodynamic interactions determine the bundling behavior. The synchronization time is smaller than the bundling time, but their ratio depends strongly on the initial separation. The bundling time decreases with increasing number of flagella at a fixed radius in a circular arrangement due to multi-helix hydrodynamics.

[1]  G. Taylor Analysis of the swimming of microscopic organisms , 1951, Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences.

[2]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[3]  H. Berg,et al.  Bacteria Swim by Rotating their Flagellar Filaments , 1973, Nature.

[4]  C. Calladine Construction of bacterial flagella , 1975, Nature.

[5]  R M Macnab,et al.  Examination of bacterial flagellation by dark-field microscopy , 1976, Journal of clinical microbiology.

[6]  C. Calladine Design requirements for the construction of bacterial flagella. , 1976, Journal of theoretical biology.

[7]  D. Tritton,et al.  Physical Fluid Dynamics , 1977 .

[8]  R M Macnab,et al.  Normal-to-curly flagellar transitions and their role in bacterial tumbling. Stabilization of an alternative quaternary structure by mechanical force. , 1977, Journal of molecular biology.

[9]  R. Macnab Bacterial flagella rotating in bundles: a study in helical geometry. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[10]  C. R. Calldine Change of waveform in bacterial flagella : the role of mechanics at the molecular level , 1978 .

[11]  J. Higdon,et al.  The hydrodynamics of flagellar propulsion: helical waves , 1979, Journal of Fluid Mechanics.

[12]  J. Higdon,et al.  A hydrodynamic analysis of flagellar propulsion , 1979, Journal of Fluid Mechanics.

[13]  H. Hotani Micro-video study of moving bacterial flagellar filaments. III. Cyclic transformation induced by mechanical force. , 1982, Journal of molecular biology.

[14]  James Lighthill,et al.  Helical distributions of stokeslets , 1996 .

[15]  E. Purcell The efficiency of propulsion by a rotating flagellum. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. Malevanets,et al.  Mesoscopic model for solvent dynamics , 1999 .

[17]  William S. Ryu,et al.  Real-Time Imaging of Fluorescent Flagellar Filaments , 2000, Journal of bacteriology.

[18]  J. M. Yeomans,et al.  Dynamics of short polymer chains in solution , 2000 .

[19]  T. Ihle,et al.  Stochastic rotation dynamics: a Galilean-invariant mesoscopic model for fluid flow. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[20]  Thomas R Powers,et al.  Role of body rotation in bacterial flagellar bundling. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  G. Huber,et al.  Periodic chirality transformations propagating on bacterial flagella. , 2002, Physical review letters.

[22]  H. Berg The rotary motor of bacterial flagella. , 2003, Annual review of biochemistry.

[23]  Howard C. Berg,et al.  E. coli in Motion , 2003 .

[24]  K. Breuer,et al.  A macroscopic scale model of bacterial flagellar bundling , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J T Padding,et al.  Hydrodynamic and brownian fluctuations in sedimenting suspensions. , 2004, Physical review letters.

[26]  MunJu Kim,et al.  Hydrodynamic interactions between rotating helices. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  R. Winkler,et al.  Dynamics of polymers in a particle-based mesoscopic solvent. , 2005, The Journal of chemical physics.

[28]  H. Noguchi,et al.  Shape transitions of fluid vesicles and red blood cells in capillary flows. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Synchronization of rotating helices by hydrodynamic interactions , 2004, The European physical journal. E, Soft matter.

[30]  G Gompper,et al.  Dynamic regimes of fluids simulated by multiparticle-collision dynamics. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  D. Fletcher,et al.  Spiroplasma Swim by a Processive Change in Body Helicity , 2005, Cell.

[32]  H. Herrmann,et al.  Simulation of claylike colloids. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  E. Lobaton,et al.  A study of bacterial flagellar bundling , 2005, Bulletin of mathematical biology.

[34]  Raymond Kapral,et al.  Two-particle friction in a mesoscopic solvent. , 2005, The Journal of chemical physics.

[35]  Raymond Kapral,et al.  Mesoscopic multiparticle collision dynamics of reaction-diffusion fronts. , 2005, The journal of physical chemistry. B.

[36]  Raymond Kapral,et al.  Mesoscopic description of solvent effects on polymer dynamics. , 2006, The Journal of chemical physics.

[37]  G. Voth,et al.  Mesoscopic modeling of bacterial flagellar microhydrodynamics. , 2006, Biophysical journal.

[38]  J. Padding,et al.  Hydrodynamic interactions and Brownian forces in colloidal suspensions: coarse-graining over time and length scales. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  J M Yeomans,et al.  Polymer packaging and ejection in viral capsids: shape matters. , 2006, Physical review letters.

[40]  J. F. Ryder,et al.  Shear thinning in dilute polymer solutions. , 2006, The Journal of chemical physics.

[41]  J. Yeomans,et al.  Hydrodynamic interaction between two swimmers at low Reynolds number. , 2007, Physical review letters.

[42]  H. Berg,et al.  Force-extension measurements on bacterial flagella: triggering polymorphic transformations. , 2007, Biophysical journal.

[43]  R. Netz,et al.  Model for self-propulsive helical filaments: kink-pair propagation. , 2007, Physical review letters.

[44]  Raymond Kapral,et al.  Chemically powered nanodimers. , 2007, Physical review letters.

[45]  Howard C. Berg,et al.  On Torque and Tumbling in Swimming Escherichia coli , 2006, Journal of bacteriology.

[46]  R. Kapral Multiparticle Collision Dynamics: Simulation of Complex Systems on Mesoscales , 2008 .

[47]  Gerhard Gompper,et al.  Direct observation of hydrodynamic instabilities in a driven non-uniform colloidal dispersion , 2008, 0810.1258.

[48]  Discrete elastic model for stretching-induced flagellar polymorphs , 2008, 0804.0893.

[49]  G. Gompper,et al.  Cooperation of sperm in two dimensions: synchronization, attraction, and aggregation through hydrodynamic interactions. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  R. Winkler,et al.  Multi-Particle Collision Dynamics -- a Particle-Based Mesoscale Simulation Approach to the Hydrodynamics of Complex Fluids , 2008, 0808.2157.

[51]  Hongyuan Jiang,et al.  Minimal model for synchronization induced by hydrodynamic interactions. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  E. Lauga,et al.  Hydrodynamic phase locking of swimming microorganisms. , 2009, Physical review letters.

[53]  R. Netz,et al.  Hydrodynamics of helical-shaped bacterial motility. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[54]  J. McWhirter,et al.  Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries , 2009, Proceedings of the National Academy of Sciences.

[55]  G. Gompper,et al.  Hydrodynamics of sperm cells near surfaces. , 2010, Biophysical journal.

[56]  Gerhard Gompper,et al.  Cell-level canonical sampling by velocity scaling for multiparticle collision dynamics simulations , 2010, J. Comput. Phys..

[57]  Gerhard Gompper,et al.  Migration of semiflexible polymers in microcapillary flow , 2010, 1006.4485.

[58]  R. Larson,et al.  The hydrodynamics of a run-and-tumble bacterium propelled by polymorphic helical flagella. , 2010, Biophysical journal.

[59]  Gerhard Gompper,et al.  Semidilute Polymer Solutions at Equilibrium and under Shear Flow , 2010, 1103.3573.

[60]  M. Graham,et al.  Coexistence of tight and loose bundled states in a model of bacterial flagellar dynamics. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[61]  L. Forró,et al.  Resonances arising from hydrodynamic memory in Brownian motion , 2011, Nature.