A model for oscillations and pattern formation in protoplasmic droplets of Physarum polycephalum

Abstract. A mechano-chemical model for the spatiotemporal dynamics of free calcium and the thickness in protoplasmic droplets of the true slime mold Physarum polycephalum is derived starting from a physiologically detailed description of intracellular calcium oscillations proposed by Smith and Saldana (Biopys. J. 61, 368 (1992)). First, we have modified the Smith-Saldana model for the temporal calcium dynamics in order to reproduce the experimentally observed phase relation between calcium and mechanical tension oscillations. Then, we formulate a model for spatiotemporal dynamics by adding spatial coupling in the form of calcium diffusion and advection due to calcium-dependent mechanical contraction. In another step, the resulting reaction-diffusion model with mechanical coupling is simplified to a reaction-diffusion model with global coupling that approximates the mechanical part. We perform a bifurcation analysis of the local dynamics and observe a Hopf bifurcation upon increase of a biochemical activity parameter. The corresponding reaction-diffusion model with global coupling shows regular and chaotic spatiotemporal behaviour for parameters with oscillatory dynamics. In addition, we show that the global coupling leads to a long-wavelength instability even for parameters where the local dynamics possesses a stable spatially homogeneous steady state. This instability causes standing waves with a wavelength of twice the system size in one dimension. Simulations of the model in two dimensions are found to exhibit defect-mediated turbulence as well as various types of spiral wave patterns in qualitative agreement with earlier experimental observation by Takagi and Ueda (Physica D, 237, 420 (2008)).

[1]  R. Rivlin Large elastic deformations of isotropic materials IV. further developments of the general theory , 1948, Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences.

[2]  T. Ueda,et al.  Propagation of phase wave in relation to tactic responses by the plasmodium of Physarum polycephalum , 1986 .

[3]  Yonosuke Kobatake,et al.  Phototaxis in true slime mold Physarum polycephalum , 1976 .

[4]  A. Tero,et al.  A coupled-oscillator model with a conservation law for the rhythmic amoeboid movements of plasmodial slime molds , 2005 .

[5]  G. Odell,et al.  Mechanics of cytogels I: oscillations in physarum. , 1984, Cell motility.

[6]  K Kurihara,et al.  Chemotaxis in Physarum polycephalum. Effects of chemicals on isometric tension of the plasmodial strand in relation to chemotactic movement. , 1976, Experimental cell research.

[7]  P K Maini,et al.  Dispersion relation in oscillatory reaction-diffusion systems with self-consistent flow in true slime mold , 2007, Journal of mathematical biology.

[8]  V. A. Teplov,et al.  A continuum model of contraction waves and protoplasm streaming in strands of Physarum plasmodium. , 1991, Bio Systems.

[9]  T. Ueda,et al.  Interaction between cell shape and contraction pattern in the Physarum plasmodium. , 2000, Biophysical chemistry.

[10]  T. Ueda,et al.  Reversal of thermotaxis with oscillatory stimulation in the plasmodium of Physarum polycephalum , 1988 .

[11]  N. Kamiya Contractile Properties of the Plasmodial Strand , 1970 .

[12]  A. Tero,et al.  Rules for Biologically Inspired Adaptive Network Design , 2010, Science.

[13]  J. Butcher Numerical Methods for Ordinary Differential Equations: Butcher/Numerical Methods , 2005 .

[14]  Einar M. Rønquist,et al.  An Operator-integration-factor splitting method for time-dependent problems: Application to incompressible fluid flow , 1990 .

[15]  Seiji Takagi,et al.  Annihilation and creation of rotating waves by a local light pulse in a protoplasmic droplet of the Physarum plasmodium , 2010 .

[16]  D. Smith,et al.  Model of the Ca2+ oscillator for shuttle streaming in Physarum polycephalum. , 1992, Biophysical journal.

[17]  Dan Luss,et al.  Impact of global interaction on pattern formation on a disk , 1995 .

[18]  George Oster,et al.  The mechanochemistry of cytogels , 1984 .

[19]  J. Butcher Numerical methods for ordinary differential equations , 2003 .

[20]  T. Nakagaki,et al.  Intelligent Behaviors of Amoeboid Movement Based on Complex Dynamics of Soft Matter , 2007 .

[21]  Werner Baumgarten,et al.  Plasmodial vein networks of the slime mold Physarum polycephalum form regular graphs. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  Jonathan Richard Shewchuk,et al.  Delaunay refinement algorithms for triangular mesh generation , 2002, Comput. Geom..

[23]  Nakagaki,et al.  Reaction-diffusion-advection model for pattern formation of rhythmic contraction in a giant amoeboid cell of the physarum plasmodium , 1999, Journal of theoretical biology.

[24]  J. Shewchuk An Introduction to the Conjugate Gradient Method Without the Agonizing Pain , 1994 .

[25]  M P Nash,et al.  Drift and breakup of spiral waves in reaction–diffusion–mechanics systems , 2007, Proceedings of the National Academy of Sciences.

[26]  T. Ueda,et al.  Emergence and transitions of dynamic patterns of thickness oscillation of the plasmodium of the true slime mold Physarum polycephalum , 2008 .

[27]  A. Tero,et al.  Mathematical Model for Rhythmic Protoplasmic Movement in the True Slime Mold , 2006, Journal of mathematical biology.

[28]  Robert D. Allen,et al.  Shuttle-Streaming: Synchronization with Heat Production in Slime Mold , 1963, Science.

[29]  S. Takagi,et al.  Locomotive mechanism of Physarum plasmodia based on spatiotemporal analysis of protoplasmic streaming. , 2008, Biophysical journal.

[30]  A F Mak,et al.  The apparent viscoelastic behavior of articular cartilage--the contributions from the intrinsic matrix viscoelasticity and interstitial fluid flows. , 1986, Journal of biomechanical engineering.

[31]  E. Alvarez-Lacalle,et al.  Global coupling in excitable media provides a simplified description of mechanoelectrical feedback in cardiac tissue. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[32]  T. Nakagaki,et al.  Pattern formation of a reaction-diffusion system with self-consistent flow in the amoeboid organism Physarum plasmodium , 1998, patt-sol/9805004.

[33]  W Alt,et al.  Cytoplasm dynamics and cell motion: two-phase flow models. , 1999, Mathematical biosciences.

[34]  H. Engel,et al.  Chemical turbulence and standing waves in a surface reaction model: The influence of global coupling and wave instabilities. , 1994, Chaos.

[35]  Alexander S. Mikhailov,et al.  Turbulence and standing waves in oscillatory chemical reactions with global coupling , 1994 .

[36]  N. Kamiya,et al.  Torsion in a protoplasmic thread. , 1954, Experimental cell research.