A Self-Organized Vortex Array of Hydrodynamically Entrained Sperm Cells

Many patterns in biological systems depend on the exchange of chemical signals between cells. We report a spatiotemporal pattern mediated by hydrodynamic interactions. At planar surfaces, spermatozoa self-organized into dynamic vortices resembling quantized rotating waves. These vortices formed an array with local hexagonal order. Introducing an order parameter that quantifies cooperativity, we found that the array appeared only above a critical sperm density. Using a model, we estimated the hydrodynamic interaction force between spermatozoa to be ∼0.03 piconewtons. Thus, large-scale coordination of cells can be regulated hydrodynamically, and chemical signals are not required.

[1]  R. Goldstein,et al.  Self-concentration and large-scale coherence in bacterial dynamics. , 2004, Physical review letters.

[2]  D. Woolley,et al.  Motility of spermatozoa at surfaces. , 2003, Reproduction.

[3]  Frank Jülicher,et al.  Membranes with rotating motors. , 2003, Physical review letters.

[4]  I. Gibbons Cilia and flagella of eukaryotes , 1981, The Journal of cell biology.

[5]  S. Leibler,et al.  Self-organization of microtubules and motors , 1997, Nature.

[6]  Ralf Lenke,et al.  Two-stage melting of paramagnetic colloidal crystals in two dimensions , 1999 .

[7]  Steven H. Strogatz,et al.  Nonlinear Dynamics and Chaos , 2024 .

[8]  J. Howard,et al.  Mechanics of Motor Proteins and the Cytoskeleton , 2001 .

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

[10]  I. Prigogine,et al.  On symmetry-breaking instabilities in dissipative systems , 1967 .

[11]  A. Libchaber,et al.  Particle diffusion in a quasi-two-dimensional bacterial bath. , 2000, Physical review letters.

[12]  H. Berg Random Walks in Biology , 2018 .

[13]  H. Moore,et al.  Exceptional sperm cooperation in the wood mouse , 2002, Nature.

[14]  S. Gueron,et al.  Computation of the internal forces in cilia: application to ciliary motion, the effects of viscosity, and cilia interactions. , 1998, Biophysical journal.

[15]  L. Fauci,et al.  Sperm motility in the presence of boundaries. , 1995, Bulletin of mathematical biology.

[16]  G. Maret,et al.  Three-particle correlations in simple liquids. , 2003, Physical review letters.

[17]  H. Berg,et al.  Moving fluid with bacterial carpets. , 2004, Biophysical journal.

[18]  Anthony A. Hyman,et al.  Rab5 regulates motility of early endosomes on microtubules , 1999, Nature Cell Biology.

[19]  Nakaoka,et al.  RECONSTITUTION OF METACHRONAL WAVES IN CILIATED CORTICAL SHEETS OF PARAMECIUM - WAVE STABILITIES , 1994, The Journal of experimental biology.

[20]  J. Gray,et al.  The Propulsion of Sea-Urchin Spermatozoa , 1955 .

[21]  M. Sleigh Cilia and flagella , 1974 .

[22]  T. Misteli The concept of self-organization in cellular architecture , 2001, The Journal of cell biology.

[23]  A. Turing The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.