Abstract
Previous models of biofilms growing in a microbial fuel cell (MFC) have primarily focused on modeling a single growth mechanism: growth via a conductive biofilm matrix, or growth utilizing diffusible electron shuttles or mediators. In this work, we implement both flavors of models in order to explore the competition for space and nutrients in a MFC biofilm populated by both species types. We find that the optimal growth conditions are for bacteria that utilize conductive EPS provided a minimal energy used to create the EPS matrix. Mediator-utilizing bacteria do have favorable niche regions, most notably close to the anode and where exposed to the bulk inflow, where oxidized mediator is readily available.
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References
Adalsteinsson D, Sethian J (1995) A fast level set method for propagating interfaces. J Comp Phys 118(2):269–277
Alpkvist E, Klapper I (2007) A multidimensional multispecies continuum model for heterogeneous biofilm development. Bull Math Biol 69:765–789
Bonanni PSP, Schrott GDG, Busalmen JPJ (2012) A long way to the electrode: how do Geobacter cells transport their electrons? Biochem Soc Trans 40(6):1274–1279
Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69(3):1548–1555
Chambless JD, Stewart PS (2007) A three-dimensional computer model analysis of three hypothetical biofilm detachment mechanisms. Biotechnol Bioeng 97(6):1573-1584
Childers SES, Ciufo SS, Lovley DRD (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416(6882):767–769
Chopp D (2001) Some improvements of the fast marching method. SIAM J Sci Comput 23:230
Duddu R, Bordas S, Chopp DL, Moran B (2008) A combined extended finite element and level set method for biofilm growth. Int J Numer Methods Eng 74(5):848–870
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
He Z, Minteer S, Angenent L (2005) Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ Sci Technol 39(14):5262–5267
Kirisits MJ, Margolis JJ, Purevdorj-Gage BL, Vaughan BL, Chopp DL, Stoodley P, Parsek MR (2007) Influence of the hydrodynamic environment on quorum sensing in Pseudomonas aeruginosa biofilms. J Bacteriol 189(22):8357–8360
Klapper I, Rupp CJ, Cargo R, Purvedorj B, Stoodley P (2002) Viscoelastic fluid description of bacterial biofilm material properties. Biotechnol Bioeng 80(3):289–296
Lee H, Torres C, Rittmann B (2009) Effects of substrate diffusion and anode potential on kinetic parameters for anode-respiring bacteria. Environ Sci Technol 43(19):7571–7577
LeVeque RJ, Li Z (1994) The immersed interface method for elliptic equations with discontinuous coefficients and singular sources. SIAM J Numer Anal 31(4):1019–1044
Lide DR (1990) CRC handbook of chemistry and physics, 70th edn. CRC Press, Boca Raton
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):5181–5192
Logan BE, Regan JM (2006) Microbial fuel cells-challenges and applications. Environ Sci Technol 40(17):5172–5180
Lovley D (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4(7):497–508
Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim B-C, Inoue K, Mester T, Covalla SF, Johnson JP, Rotello VM, Tuominen MT, Lovley DR (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6(9):573–579
Marcus A, Torres C, Rittmann B (2010) Evaluating the impacts of migration in the biofilm anode using the model PCBIOFILM. Electrochim Acta 55:6964–6972
Marcus A, Torres C, Rittmann B (2011) Analysis of a microbial electrochemical cell using the proton condition in biofilm (PCBIOFILM) model. Bioresour Technol 102(1):253–262
Marcus AK, Torres CI, Rittmann BE (2007) Conduction-based modeling of the biofilm anode of a microbial fuel cell. Biotechnol Bioeng 98(6):1171–1182
Merkey BV, Chopp DL (2012) The performance of a microbial fuel cell depends strongly on anode geometry: a multidimensional modeling study. Bull Math Biol 74:834–857
Merkey BV, Rittmann BE, Chopp DL (2009) Modeling how soluble microbial products (SMP) support heterotrophic bacteria in autotroph-based biofilms. J Theor Biol 259(4):670–683
Min B, Kim J, Oh S, Regan J, Logan B (2005) Electricity generation from swine wastewater using microbial fuel cells. Water Res 39(20):4961–4968
Morgenroth E, Wilderer PA (2000) Influence of detachment mechanisms on competition in biofilms. Water Res 34(2):417–426
Osher S, Sethian J (1988) Fronts propagating with curvature-dependent speed: algorithms based on Hamilton–Jacobi formulations. J Comput Phys 79(1):12–49
Picioreanu C, Head IM, Katuri KP, van Loosdrecht MC, Scott K (2007a) A computational model for biofilm-based microbial fuel cells. Water Res 41:2921–2940
Picioreanu C, Katuri K, van Loosdrecht M, Head I, Scott K (2010a) Modelling microbial fuel cells with suspended cells and added electron transfer mediator. J Appl Electrochem 40(1):151–162
Picioreanu C, Kreft JU, Klausen M, Haagensen JAJ, Tolker-Nielsen T, Molin S (2007b) Microbial motility involvement in biofilm structure formation-a 3D modelling study. Water Sci Technol 55(8–9):337–343
Picioreanu C, van Loosdrecht M, Curtis T, Scott K (2010b) Model based evaluation of the effect of pH and electrode geometry on microbial fuel cell performance. Bioelectrochemistry 78(1):8–24
Picioreanu C, van Loosdrecht MC, Heijnen JJ (1999) Discrete-differential modelling of biofilm structure. Water Sci Technol 39(7):115–122
Picioreanu C, van Loosdrecht MC, Heijnen JJ (2001) Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. Biotechnol Bioeng 72(2):205–218
Rabaey K, Verstraete W (2005) Microbial fuel cells: novel biotechnology for energy generation. TRENDS Biotechnol 23(6):291–298
Reguera G, McCarthy K, Mehta T, Nicoll J, Tuominen M, Lovley D (2005) Extracellular electron transfer via microbial nanowires. Nature 435(7045):1098–1101
Reguera G, Nevin K, Nicoll J, Covalla S, Woodard T, Lovley D (2006a) Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72(11):7345
Reguera G, Pollina R, Nicoll J, Lovley D (2006b) Possible non-conductive role of Geobacter sulfurreducens pili nanowires in biofilm formation. J Bacteriol 189(5):2125–2127
Renslow RS, Babauta JT, Dohnalkova AC, Boyanov MI, Kemner KM, Majors PD, Fredrickson JK, Beyenal H (2013) Metabolic spatial variability in electrode-respiring Geobacter sulfurreducens biofilms. Energy Environ Sci 6(6):1827
Rittmann BE (1982) The effect of shear stress on biofilm loss rate. Biotechnol Bioeng 24(2):501–506
Rittmann BE, Torres CI, Marcus AK (2008) Understanding the distinguishing features of a microbial fuel cell as a biomass-based renewable energy technology. In: Shah V (ed) Emerging environmental technologies. Springer, New York, pp 1–28
Smith BG, Vaughan BL, Chopp DL (2007) The eXtended finite element method for boundary layer problems in biofilm growth. Commun Appl Math Comput Sci 2(1):35–56
Stewart P (2003) Diffusion in biofilms. J Bacteriol 185(5):1485
Torres C, Marcus A, Lee H, Parameswaran P, Krajmalnik-Brown R, Rittmann B (2010) A kinetic perspective on extracellular electron transfer by anode-respiring bacteria. FEMS Microbiol Rev 34(1):3–17
Torres C, Marcus A, Parameswaran P, Rittmann B (2008) Kinetic experiments for evaluating the Nernst–Monod model for anode-respiring bacteria (ARB) in a biofilm anode. Environ Sci Technol 42(17):6593–6597
Vaughan B, Smith B, Chopp D (2010) The influence of fluid flow on modeling quorum sensing in bacterial biofilms. Bull Math Biol 72:1143–1165
Vaughan BL, Smith BG, Chopp DL (2006) A comparison of the eXtended finite element method with the immersed interface method for elliptic equations with discontinuous coefficients and singular sources. Commun Appl Math Comput Sci 1(1):207–228
Wanner O, Eberl H, van Loosdrecht M, Morgenroth E, Noguera D, Picioreanu C, Rittmann B (2006) Mathematical modeling of biofilms. Technical report, International Water Association
Wanner O, Gujer W (1986) A multispecies biofilm model. Biotechnol Bioeng 28:314–328
Wäsche S, Horn H, Hempel DC (2002) Influence of growth conditions on biofilm development and mass transfer at the bulk/biofilm interface. Water Res 36(19):4775–4784
Xavier J, de Kreuk MK, Picioreanu C, van Loosdrecht MC (2007) Multi-scale individual-based model of microbial and bioconversion dynamics in aerobic granular sludge. Environ Sci Technol 41:6410–6417
Xavier J, Picioreanu C, van Loosdrecht MC (2005) A general description of detachment for multidimensional modelling of biofilms. Biotechnol Bioeng 91(6):651–669
Xavier J, Foster KR (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104(3):876–881
Zhang TC, Fu Y-C, Bishop PL (1995) Competition for substrate and space in biofilms. Water Environ Res 67(6):992–1003
Acknowledgments
We want to thank Bruce Rittmann at Arizona State University for helpful discussions regarding this work. This work was supported by the NSF (Grant DMS-0921015) and the Initiative for Sustainability and Energy at Northwestern University (ISEN).
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Merkey, B.V., Chopp, D.L. Modeling the Impact of Interspecies Competition on Performance of a Microbial Fuel Cell. Bull Math Biol 76, 1429–1453 (2014). https://doi.org/10.1007/s11538-014-9968-0
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DOI: https://doi.org/10.1007/s11538-014-9968-0