Skip to main content
Log in

A Mixed-Culture Biofilm Model with Cross-Diffusion

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

We propose a deterministic continuum model for mixed-culture biofilms. A crucial aspect is that movement of one species is affected by the presence of the other. This leads to a degenerate cross-diffusion system that generalizes an earlier single-species biofilm model. Two derivations of this new model are given. One, like cellular automata biofilm models, starts from a discrete in space lattice differential equation where the spatial interaction is described by microscopic rules. The other one starts from the same continuous mass balances that are the basis of other deterministic biofilm models, but it gives up a simplifying assumption of these models that has recently been criticized as being too restrictive in terms of ecological structure. We show that both model derivations lead to the same PDE model, if corresponding closure assumptions are introduced. To investigate the role of cross-diffusion, we conduct numerical simulations of three biofilm systems: competition, allelopathy and a mixed system formed by an aerobic and an anaerobic species. In all cases, we find that accounting for cross-diffusion affects local distribution of biomass, but it does not affect overall lumped quantities such as the total amount of biomass in the system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Almeida C, Azevedo NF, Santos S, Keevil CW, Vieira MJ (2011) Discriminating multi-species populations in biofilms with peptide nucleic acid fluorescence in situ hybridization (PNA FISH). Plos ONE 6(3):e14786

    Article  Google Scholar 

  • Alpkvist E, Klapper I (2007) A multidimensional multispecies continuum model for heterogeneous biofilm development. Bull Math Biol 69(2):765789

    Google Scholar 

  • Anguige K, King JR, Ward JP (2005) Modelling antibiotic- and anti-quorum sensing treatment of a spatially-structured Pseudomonas aeruginosa population. J Math Biol 51:557–594

    Article  MathSciNet  MATH  Google Scholar 

  • Anguige K, Schmeiser C (2009) A one-dimensional model of cell-diffusion and aggregation, incorporating volume filling and cell-to-cell adhesion. J Math Biol 58:395–427

    Article  MathSciNet  MATH  Google Scholar 

  • Bryers JD, Drummond F (1998) Local macromolecule diffusion coefficients in structurally non-uniform bacterial biofilms using fluorescence recovery after photobleaching (FRAP). Biotechnol Bioeng 60(4):462–473

    Article  Google Scholar 

  • Chambless JD, Hunt SM, Stewart PS (2006) A three-dimensional computer model of four hypothetical mechanisms protecting biofilms from antimicrobials. Appl Environ Mivrobiol 72(3):2005–2013

    Article  Google Scholar 

  • Clarelli F, Di Russo C, Natalini R, Ribot M (2013) A fluid dynamics model of the growth of phototrophic biofilms. J Math Biol 66(7):1387–1408

    Article  MathSciNet  MATH  Google Scholar 

  • Cogan NG (2008) Two-fluid model of biofilm disinfection. Bull Math Biol 70:800–819

    Article  MathSciNet  MATH  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 248(5418):13181322

    Google Scholar 

  • Cumsille P, Asenjoc JA, Concad C (2014) A novel model for biofilm growth and its resolution by using the hybrid immersed interface-level set method. Comput Math Appl 67(1):34–51

    Article  MathSciNet  Google Scholar 

  • Dockery J, Klapper I (2001) Finger formation in biofilm layers. SIAM J Appl Math 62(3):853–869

    MathSciNet  MATH  Google Scholar 

  • Duddu R, Chopp DL, Moran B (2009) A two-dimensional continuum model of biofilm growth incorporating fluid flow and shear stress based detachment. Biotechnol Bioeng 103(1):92–104

    Article  Google Scholar 

  • Eberl HJ, Demaret L (2007) A finite difference scheme for a doubly degenerate diffusion–reaction equation arising in microbial ecology. J Differ Equ CS15:77–95

    MathSciNet  Google Scholar 

  • Eberl HJ, Sudarsan R (2008) Exposure of biofilms to slow flow fields: the convective contribution to growth and disinfection. J Theor Biol 253(4):788–807

    Article  MathSciNet  Google Scholar 

  • Eberl HJ, Collinson MS (2009) A modeling and simulation study of siderophore mediated antagonism in dual-species biofilms. Theor Biol Med Mod 6:30

    Article  Google Scholar 

  • Eberl H, Parker DF, van Loosdrecht MCM (2001) A new deterministic spatio-temporal continuum model for biofilm development. J Theor Med 3:161–175

    Article  MATH  Google Scholar 

  • Eberl HJ, Khassekhan H, Demaret L (2010) A mixed-culture model of a probiotic biofilm control system. Comput Math Methods Med 11(2):99–118

    Article  MathSciNet  MATH  Google Scholar 

  • Efendiev MA, Eberl HJ, Zelik SV (2002) Existence and longtime behavior of solutions of a nonlinear reaction–diffusion system arising in the modeling of biofilms. RIMS Kyoto Kokyuroko 1258:49–71

    MathSciNet  Google Scholar 

  • Efendiev MA, Zelik SV, Eberl HJ (2009) Existence and longtime behavior of a biofilm Model. Commun Pure Appl Math 8(2):509–531

    MathSciNet  MATH  Google Scholar 

  • Emerenini BO, Hense BA, Kuttler C, Eberl HJ (2015) A mathematical model of quorum sensing induced biofilm detachment. Plos ONE 10(7):e0132385

    Article  Google Scholar 

  • Fratamico PM, Annous BA, Gunther NW IV (eds) (2009) Biofilms in the food and beverage industries. Woodhead Publishing, CRC Press, Boca Raton

    Google Scholar 

  • Fgaier H, Kalmokoff M, Ells T, Eberl HJ (2014) An allelopathy based model for the Listeria overgrowth phenomenon. Math Biosci 247:13–26

    Article  MathSciNet  MATH  Google Scholar 

  • Frederick MR, Kuttler C, Hense BA, Eberl HJ (2011) A mathematical model of quorum sensing regulated EPS production in biofilm communities. Theor Biol Med Model 8:8

    Article  Google Scholar 

  • Frederick MR, Kuttler C, Hense BA, Müller J, Eberl HJ (2010) A mathematical model of quorum sensing in patchy biofilm communities with slow background flow. Can Appl Math Q 18(3):267–298

    MathSciNet  MATH  Google Scholar 

  • Friedman A, Hu B, Xue C (2014) On a multiphase multicomponent model of biofilm growth. Arch Ration Mech Anal 211(1):257–300

    Article  MathSciNet  MATH  Google Scholar 

  • Hunt SM, Werner EM, Huang B, Hamilton MA, Stewart PS (2004) Hypothesis for the role of nutrient starvation in biofilm detachment. Appl Environ Microbiol 70:7418–7425

    Article  Google Scholar 

  • Hunt SM, Hamilton MA, Stewart PS (2005) A 3D model of antimicrobial action on biofilms. Water Sci Technol 52(7):143–148

    Google Scholar 

  • Jalbert E, Eberl HJ (2014) Numerical computation of sharp travelling waves of a degenerate diffusion-reaction equation arising in biofilm modelling. Commun Nonlinear Sci Numer Sim 19(7):2181–2190

    Article  MathSciNet  Google Scholar 

  • Kepka G (2008) Interaction of Pseudomonas putida and Listeria monocytogenes in mixed culture biofilms. M.Sc. thesis, Lakehead University

  • Khassehkhan H, Efendiev MA, Eberl HJ (2009a) A degenerate diffusion reaction model of an amensalistic probiotic biofilm control system: existence and simulation of solutions. Discrete Contin Dyn Syst B 12(2):371–388

    Article  MathSciNet  MATH  Google Scholar 

  • Khassehkhan H, Hillen T, Eberl HJ (2009b) A nonlinear master equation for a degenerate diffusion model of biofilm growth. LNCS, vol. 5544, pp. 735–744

  • Klapper I, Dockery J (2010) Mathematical description of microbial biofilms. SIAM J Appl Math 52(2):221265

    MathSciNet  Google Scholar 

  • Klapper I, Szomolay B (2011) An exclusion principle and the importance of mobility for a class of biofilm models. Bull Math Biol 73(9):2213–2230

    Article  MathSciNet  MATH  Google Scholar 

  • Koza A, Hallett PD, Moon CD, Spiers AJ (2009) Characterization of a novel air–liquid interface biofilm of Pseudomonas fluorescens SBW25. Microbiology 155(5):1397–1406

    Article  Google Scholar 

  • Kreft J-U (2004) Biofilms promote altruism. Microbiology 150(8):2751–2760

    Article  Google Scholar 

  • Lewandowski Z (2011) Biofilms in water and wastewater treatment. In: Wilderer P (ed) Treatise on water science. Elsevier, Amsterdam, pp 529–570

    Chapter  Google Scholar 

  • Lewandowski Z, Beyenal H (2007) Fundamentals of biofilm research. CRC Press, Boca Raton

    Book  Google Scholar 

  • Lizavan M, Padorn V (1999) A spatially discrete model of aggregating populations. J Math Biol 38:79–102

    Article  MathSciNet  Google Scholar 

  • Logan BE, Hamelers B, Rozendal R, Schroder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40(17):51815192

    Google Scholar 

  • Lindley B, Wang Q, Zhang T (2011) A multicomponent model for biofilm–drug interaction. DCDS-B 15(2):417–456

    Article  MathSciNet  MATH  Google Scholar 

  • Merkey BV, Chopp DL (2014) Modeling the impact of interspecies competition on performance of a microbial fuel cell. Bull Math Biol 76(6):1429–1453

    Article  MathSciNet  MATH  Google Scholar 

  • Merkey BV, Rittman BE, Chopp DL (2009) Modeling how soluble microbial products (SMP) support heterotrophic bacteria in autotroph-based biofilms. J Theor Biol 259(4):670–683

    Article  Google Scholar 

  • Muhammad N, Eberl HJ (2010) OpenMP parallelization of a Mickens time-integration scheme for a mixed-culture biofilm model and its performance on multi-core and multi-processor computers. LNCS, vol. 5976, pp. 180–195

  • Muhammad N, Eberl HJ (2011) Model parameter uncertainties in a dual-species biofilm competition model affect ecological output parameters much stronger than morphological ones. Math Biosci 233(1):1–18

    Article  MathSciNet  MATH  Google Scholar 

  • Nielsen AT, Tolker-Nielsen T, Barken KB, Molin S (2000) Role of commensal relationships on the spatial structure of a surface-attached microbial consortium. Environ Microbiol 2(1):59–68

    Article  Google Scholar 

  • Noguera DR, Pizarro G, Stahl DA, Rittmann BE (1999) Simulation of multispecies biofilm development in three dimensions. Water Sci Technol 39(7):123–130

    Article  Google Scholar 

  • Okubo A, Levin SA (1980) Diffusion in ecological problems: modern perspectives, 2nd edn. Springer, Berlin

    Google Scholar 

  • Ostrander S (2011) Macroscopic cross-diffusion models derived from spatially discrete continuous time microscopic models. SIAM SIURO. doi:10.1137/10S010818

    Google Scholar 

  • Painter K, Hillen T (2002) Volume-filling and quorum sensing in models for chemosensitive movement. Can Appl Math Q 10:501–543

    MathSciNet  MATH  Google Scholar 

  • Picioreanu C, van Loosdrecht MCM, Heijnen JJ (1998) A new combined differential-discrete cellular automaton approach for biofilm modeling: application for growth in gel beads. Biotechnol Bioeng 57(6):718–731

    Article  Google Scholar 

  • Picioreanu C, Kreft J, van Loosdrecht MCM (2004) Particle-based multidimensional multispecies biofilm model. Appl Environ Microbiol 70(5):3024–3040

    Article  Google Scholar 

  • Prieto-Langarica A, Kojouharov HV, Chen-Charpentier BM (2012a) Discrete and continuous approaches to modeling cell movement in the presence of a foreign stimulus. Comput Math Appl 64(3):167–174

    Article  MathSciNet  MATH  Google Scholar 

  • Prieto-Langarica A, Kojouharov HV, Chen-Charpentier BM (2012b) Upscaling from discrete to continuous mathematical models of two interacting populations. Comput Math Appl 66(9):1606–1612

    Article  MathSciNet  Google Scholar 

  • Purevdorj-Gage B, Costerton WJ, Stoodley P (2005) Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology 151:1569–1576

    Article  Google Scholar 

  • Rahman KA, Eberl HJ (2014) Numerical treatment of a cross-diffusion model of biofilm exposure to antimicrobials. LNCS 8384:134–144

    MathSciNet  Google Scholar 

  • Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill, New York

    Google Scholar 

  • Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184(1140–1154):2001

    Google Scholar 

  • Seminara A, Angelini TE, Wilking JN, Vlamakis H, Ebrahim S, Kolter R, Weitz DA, Brenner MP (2012) Osmotic spreading of Bacillus subtilis biofilms driven by an extracellular matrix. PNAS 109(4):116–1121

    Article  Google Scholar 

  • Shigesada N, Kawasaki K, Teramoto E (1979) Spatial segregation of interacting species. J Theor Biol 79(1):83–99

    Article  MathSciNet  Google Scholar 

  • Sonner S, Efendiev MA, Eberl HJ (2011) On the well-posedness of a mathematical model of quorum-sensing in patchy biofilm communities. Math Methods Appl Sci 34(13):1667–1684

    Article  MathSciNet  MATH  Google Scholar 

  • Sneddon IA (1961) Special functions of mathematical physics and chemistry. Oliver & Boyd, Edinburgh

    Google Scholar 

  • Stevens A, Othmer HG (1997) Aggregation, blowup, and collapse: the ABC’s of taxis in reinforced random walks. SIAM J Appl Math 57(4):10441081

    Article  MathSciNet  Google Scholar 

  • Stewart PS (2003) Diffusion in biofilms. J Bacteriol 185:1485–1491

    Article  Google Scholar 

  • Tan S, Yu T, Shi H-C (2014) Microsensor determination of multiple microbial processes in an oxygen-based membrane aerated biofilm. Water Sci Technol 69(5):909–914

    Article  Google Scholar 

  • Tang Y, Valocchi AJ (2013) An improved cellular automaton method to model multispecies biofilms. Water Res 47:5729–5742

    Article  Google Scholar 

  • Terada A, Lackner S, Kristensen K, Smets BF (2010) Inoculum effects on community composition and nitration performance of autotrophic nitrifying biofilm reactors with counter-diffusion geometry. Environ Microbiol 12(10):2858–2872

    Google Scholar 

  • Tolker-Nielsen T, Molin S (2000) Spatial organization of microbial biofilm communities. Microb Ecol 40(2):75–84

    Google Scholar 

  • Turner S, Sherratt JA, Painter KJ (2004) From a discrete to a continuous model of biological cell movement. Phys Rev E 69:1–10

    Article  MathSciNet  Google Scholar 

  • van Loosdrecht MCM, Heijnen JJ, Eberl H, Kreft J, Picioreanu C (2002) Mathematical modelling of biofilms structures. Antonie van Leeuwenhoek 81:245–256

    Article  Google Scholar 

  • Vaughan BL, Smith BG, Chopp DL (2010) The influence of fluid flow on modeling quorum sensing in bacterial biofilms. Bull Math Biol 72(5):1143–1165

    Article  MATH  Google Scholar 

  • Visser AW (2008) Lagrangian modelling of plankton motion: from deceptively simple random walks to Fokker–Planck and back again. J Mar Sys 70:287–299

    Article  Google Scholar 

  • Wang R, Terada A, Lackner S, Smets BF, Henze M, Xia S, Zhao J (2009) Nitration performance and biofilm development of co- and counter-diffusion biofilm reactors: modeling and experimental comparison. Water Res 43:2699–2709

    Article  Google Scholar 

  • Wanner O, Gujer W (1986) A multispecies biofilm model. Biotechnol Bioeng 28(3):314–328

    Article  Google Scholar 

  • Wanner O, Eberl H, Morgenroth E, Noguera D, Picioreanu C, Rittmann B, van Loosdrecht M (2006) Mathematical modeling of biofilms. IWA Publishing, London

    Google Scholar 

  • Ward JP, King JR (2012) Thin-film modelling of biofilm growth and quorum sensing. J Eng Math 73(1):71–92

    Article  MathSciNet  Google Scholar 

  • Wood BD, Whitaker S (1999) Cellular growth in biofilms. Biotechnol Bioeng 64(6):656–670

    Article  Google Scholar 

  • Xavier JB, Picioreanu C, van Loosdrecht MCM (2005) A framework for multidimensional modelling of activity and structure of multispecies biofilms. Environ Microbiol 7(8):1085–1103

    Article  Google Scholar 

  • Xavier JB, Picioreanu C, van Loosdrecht MCM (2004) A modelling study of the activity and structure of biofilms in biological reactors. Biofilms 1(4):377–391

    Article  Google Scholar 

  • Zhang T (2012) Modeling of biocide action against biofilm. Bull Math Biol 74:1427–1447

    Article  MathSciNet  MATH  Google Scholar 

  • Zhang T, Cogan NG, Wang Q (2008) Phase-field models for biofilms II. 2-D numerical simulations of biofilm-flow interaction. Commun Comput Phys 4(1):72–101

    Google Scholar 

Download references

Acknowledgments

This study was support by the Natural Science and Engineering Research Council of Canada (NSERC) under a Discovery Grant awarded to HJE and by the Canada Research Chairs Program. The computing equipment used in this study was a SGI Altix 450 funded by the Canada Foundation for Innovation through a New Leaders Opportunity Grant and operated by SHARCNET, an SGI Altix UV and custom-built Intel Xeon workstation funded by NSERC through a Research Tool and Infrastructure Grant and operated by the Department of Mathematics and Statistics. The authors thank Kaizaad Bilimorya (SHARCNET) and Larry Banks (Dept. Math & Stats) for the technical support. The authors thank Greg Kepka (Lakehead University) for providing the CLSM images.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hermann J. Eberl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 741 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahman, K.A., Sudarsan, R. & Eberl, H.J. A Mixed-Culture Biofilm Model with Cross-Diffusion. Bull Math Biol 77, 2086–2124 (2015). https://doi.org/10.1007/s11538-015-0117-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-015-0117-1

Keywords

Mathematics Subject Classification

Navigation