Spatially Heterogeneous Biofilm Simulations using an Immersed Boundary Method with Lagrangian Nodes Defined by Bacterial Locations

In this work we consider how surface-adherent bacterial biofilm communities respond in flowing systems. We simulate the fluid-structure interaction and separation process using the immersed boundary method. In these simulations we model and simulate different density and viscosity values of the biofilm than that of the surrounding fluid. The simulation also includes breakable springs connecting the bacteria in the biofilm. This allows the inclusion of erosion and detachment into the simulation. We use the incompressible Navier-Stokes (N-S) equations to describe the motion of the flowing fluid. We discretize the fluid equations using finite differences and use a geometric multigrid method to solve the resulting equations at each time step. The use of multigrid is necessary because of the dramatically different densities and viscosities between the biofilm and the surrounding fluid. We investigate and simulate the model in both two and three dimensions. Our method differs from previous attempts of using IBM for modeling biofilm/flow interactions in the following ways: the density and viscosity of the biofilm can differ from the surrounding fluid, and the Lagrangian node locations correspond to experimentally measured bacterial cell locations from 3D images taken of Staphylococcus epidermidis in a biofilm.

[1]  T. R. Bott,et al.  Direct measurement of the adhesive strength of biofilms in pipes by micromanipulation , 1998 .

[2]  H. Sung,et al.  An immersed boundary method for fluid–flexible structure interaction , 2009 .

[3]  M. Minion,et al.  Accurate projection methods for the incompressible Navier—Stokes equations , 2001 .

[4]  D. Bottino,et al.  Modeling Viscoelastic Networks and Cell Deformation in the Context of the Immersed Boundary Method , 1998 .

[5]  C. Peskin Numerical analysis of blood flow in the heart , 1977 .

[6]  C. Laspidou,et al.  On the calculation of the elastic modulus of a biofilm streamer. , 2008, Biotechnology and bioengineering.

[7]  G. Booth,et al.  BacSim, a simulator for individual-based modelling of bacterial colony growth. , 1998, Microbiology.

[8]  Laura Guglielmini,et al.  Laminar flow around corners triggers the formation of biofilm streamers , 2010, Journal of The Royal Society Interface.

[9]  C. Peskin,et al.  Implicit second-order immersed boundary methods with boundary mass , 2008 .

[10]  Rajat Mittal,et al.  An immersed-boundary method for flow-structure interaction in biological systems with application to phonation , 2008, J. Comput. Phys..

[11]  William L. Briggs,et al.  A multigrid tutorial , 1987 .

[12]  J J Heijnen,et al.  Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. , 2001, Biotechnology and bioengineering.

[13]  Wanda Strychalski,et al.  Viscoelastic Immersed Boundary Methods for Zero Reynolds Number Flow , 2012 .

[14]  Tianyu Zhang,et al.  Review of mathematical models for biofilms , 2010 .

[15]  C. Peskin The immersed boundary method , 2002, Acta Numerica.

[16]  Arnold Neumaier,et al.  Introduction to Numerical Analysis , 2001 .

[17]  J W Wimpenny,et al.  Individual-based modelling of biofilms. , 2001, Microbiology.

[18]  Cory J. Rupp,et al.  Viscoelastic fluid description of bacterial biofilm material properties. , 2002, Biotechnology and bioengineering.

[19]  Robert Michael Kirby,et al.  Unconditionally stable discretizations of the immersed boundary equations , 2007, J. Comput. Phys..

[20]  Leonid Pavlovsky,et al.  In situ rheology of Staphylococcus epidermidis bacterial biofilms. , 2013, Soft matter.

[21]  M. Spiga,et al.  A symmetric solution for velocity profile in laminar flow through rectangular ducts , 1994 .

[22]  C. Peskin,et al.  Simulation of a Flapping Flexible Filament in a Flowing Soap Film by the Immersed Boundary Method , 2002 .

[23]  H. Darmani Todar's Online Textbook of Bacteriology , 2006 .

[24]  Ronald Fedkiw,et al.  The immersed interface method. Numerical solutions of PDEs involving interfaces and irregular domains , 2007, Math. Comput..

[25]  Perry L. McCarty,et al.  Evaluation of steady‐state‐biofilm kinetics , 1980 .

[26]  M. Minion,et al.  The Blob Projection Method for Immersed Boundary Problems , 2000 .

[27]  Paul Stoodley,et al.  Viscoelasticity of Staphylococcus aureus Biofilms in Response to Fluid Shear Allows Resistance to Detachment and Facilitates Rolling Migration , 2005, Applied and Environmental Microbiology.

[28]  Zhibing Zhang,et al.  Effects of operating conditions on the adhesive strength of Pseudomonas fluorescens biofilms in tubes. , 2005, Colloids and surfaces. B, Biointerfaces.

[29]  M. Zamir,et al.  The Physics of Pulsatile Flow , 2000, Biological Physics Series.

[30]  R. Dillon,et al.  Using the immersed boundary method to model complex fluids-structureinteraction in sperm motility , 2010 .

[31]  J J Heijnen,et al.  Effect of diffusive and convective substrate transport on biofilm structure formation: a two-dimensional modeling study. , 2000, Biotechnology and bioengineering.

[32]  Robert L. Street,et al.  Numerical Simulation of Mixed-Culture Biofilm , 1984 .

[33]  Qi Wang,et al.  Phase Field Models for Biofilms. I. Theory and One-Dimensional Simulations , 2008, SIAM J. Appl. Math..

[34]  B. Rittmann,et al.  Comparative performance of biofilm reactor types , 1982, Biotechnology and bioengineering.

[35]  Tianyu Zhang,et al.  Phase-Field Models for Biofilms II. 2-D Numerical Simulations of Biofilm-Flow Interaction , 2008 .

[36]  J. Dutcher,et al.  Absolute quantitation of bacterial biofilm adhesion and viscoelasticity by microbead force spectroscopy. , 2009, Biophysical journal.

[37]  Y. Watanabe,et al.  Biofilm Properties and Simultaneous Nitrification and Denitrification in Aerobic Rotating Biological Contactors , 1991 .

[38]  I. Klapper,et al.  Description of mechanical response including detachment using a novel particle model of biofilm/flow interaction. , 2007, Water science and technology : a journal of the International Association on Water Pollution Research.

[39]  Isaac Klapper,et al.  Mathematical Description of Microbial Biofilms , 2010, SIAM Rev..

[40]  Cristian Picioreanu,et al.  Particle-Based Multidimensional Multispecies Biofilm Model , 2004, Applied and Environmental Microbiology.

[41]  Randall J. LeVeque,et al.  Finite difference methods for ordinary and partial differential equations - steady-state and time-dependent problems , 2007 .

[42]  J. Ghigo,et al.  The characterization of functions involved in the establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides. , 2008, Environmental microbiology.

[43]  Robert Dillon,et al.  Modeling Biofilm Processes Using the Immersed Boundary Method , 1996 .

[44]  R. Hozalski,et al.  Development and testing of a novel microcantilever technique for measuring the cohesive strength of intact biofilms , 2010, Biotechnology and bioengineering.