×

Analysis and simulations of a free boundary problem modelling phototrophic granular biofilms. (English) Zbl 07922078

Summary: A model simulating the initial formation and growth of a phototrophic granular biofilm around wireless light emitter is proposed. The work focuses on the well-posedness and quantitative analysis of the model describing the initiation of the biofilm growth induced by cell attachment in the case of spherical geometry. Biofilm granule generates from the agglomeration of free living cells which lead to the formation of spherical-shaped microbial consortia. Under the hypothesis of radial symmetry, the granular biofilm is modelled as a free boundary domain, where the free boundary is the radius of the granule. The attached species proliferate by consuming dissolved substrates diffusively transported from the bulk liquid within the granule. Granule size evolves over time due to attachment flux, microbial growth and invasion. The evolution of the state variables, that is the concentrations of the microbial cells both in sessile and suspended form and the dissolved substrates, is governed by a nonlinear system of hyperbolic-elliptic differential equations, while the free boundary evolution is governed by an ordinary differential equation. Light intensity provided by the emitter is accounted in the model as a further state variable, as it affects the attachment velocity and metabolic activity of light-dependent microorganisms. By using the method of characteristics, the equations are converted into an equivalent integral system. Existence and uniqueness of solutions are discussed and proved for the attachment regime using fixed point strategies. A numerical study is performed to explore and investigate the role of light-dependent species on the granulation process and how light conditions and concentration of nutrients affect the attachment and granule initiation.

MSC:

35R35 Free boundary problems for PDEs
35L45 Initial value problems for first-order hyperbolic systems
35Bxx Qualitative properties of solutions to partial differential equations
92B05 General biology and biomathematics
Full Text: DOI

References:

[1] A. S. Abouhend, K. Milferstedt, J. Hamelin, A. A. Ansari, C. Butler, B. I. Carbajal-González and C. Park, Growth progression of oxygenic photogranules and its impact on bioactivity for aeration-free wastewater treatment, Environmental Science Technology, 54 (2019), 486-496.
[2] E. Alpkvist and I. Klapper, A multidimensional multispecies continuum model for heterogeneous biofilm development, Bulletin of Mathematical Biology, 69 (2007), 765-789. · Zbl 1138.92371
[3] Y. H. An and R. J. Friedman, Concise review of mechanisms of bacterial adhesion to biomaterial surfaces, Journal of Biomedical Materials research, 43 (1998), 338-348.
[4] J. E. Baeten, D. J. Batstone, O. J. Schraa, M. C. van Loosdrecht and E. I. Volcke, Modelling anaerobic, aerobic and partial nitritation-anammox granular sludge reactors-A review, Water Research, 149 (2019), 32-341.
[5] D. J. Batstone, J. Keller and L. L. Blackall, The influence of substrate kinetics on the microbial community structure in granular anaerobic biomass, Water Research, 38 (2004), 1390-1404.
[6] R. Bianchini and R. Natalini, Global existence and asymptotic stability of smooth solutions to a fluid dynamics model of biofilms in one space dimension, Journal of Mathematical Analysis and Applications, 434 (2016), 1909-1923. doi: 10.1016/j.jmaa.2015.10.014. · Zbl 1330.35312 · doi:10.1016/j.jmaa.2015.10.014
[7] F. Clarelli, C. Di Russo, R. Natalini and M. Ribot, A fluid dynamics model of the growth of phototrophic biofilms, Journal of Mathematical Biology, 66 (2013), 1387-1408. doi: 10.1007/s00285-012-0538-5. · Zbl 1264.92048 · doi:10.1007/s00285-012-0538-5
[8] G. M. Coclite, M. M. Coclite and S. Mishra, On a model for the evolution of morphogens in a growing tissue, SIAM Journal on Mathematical Analysis, 48 (2016), 1575-1615. doi: 10.1137/15M1037524. · Zbl 1381.35186 · doi:10.1137/15M1037524
[9] B. D’Acunto and L. Frunzo, Qualitative analysis and simulations of a free boundary problem for multispecies biofilm models, Mathematical and Computer modelling, 53 (2011), 1596-1606. doi: 10.1016/j.mcm.2010.12.024. · Zbl 1219.35324 · doi:10.1016/j.mcm.2010.12.024
[10] B. D’Acunto, L. Frunzo, V. Luongo and M. R. Mattei, Free boundary approach for the attachment in the initial phase of multispecies biofilm growth, Zeitschrift für Angewandte Mathematik und Physik, 70 (2019), 1-16. doi: 10.1007/s00033-019-1134-y. · Zbl 1415.35293 · doi:10.1007/s00033-019-1134-y
[11] B. D’Acunto, L. Frunzo, V. Luongo, M. R. Mattei and A. Tenore, Free boundary problem for the role of planktonic cells in biofilm formation and development, Z. Angew. Math. Phys., 72 (2021), 1-17. doi: 10.1007/s00033-021-01561-3. · Zbl 1477.35283 · doi:10.1007/s00033-021-01561-3
[12] B. D’Acunto, L. Frunzo and M. R. Mattei, Moving boundary problem for the detachment in multispecies biofilms, Ricerche di Matematica, 67 (2018), 683-698. doi: 10.1007/s11587-017-0333-0. · Zbl 1516.35563 · doi:10.1007/s11587-017-0333-0
[13] M. De Angelis and G. Fiore, Existence and uniqueness of solutions of a class of third order dissipative problems with various boundary conditions describing the Josephson effect, Journal of Mathematical Analysis and Applications, 404 (2013), 477-490. doi: 10.1016/j.jmaa.2013.03.029. · Zbl 1310.35077 · doi:10.1016/j.jmaa.2013.03.029
[14] C. Di Iaconi, R. Ramadori, A. Lopez and R. Passino, Influence of hydrodynamic shear forces on properties of granular biomass in a sequencing batch biofilter reactor, Biochemical Engineering Journal, 30 (2006), 152-157.
[15] A. Doloman, H. Varghese, C. D. Miller and N. S. Flann, Modeling de novo granulation of anaerobic sludge, BMC Systems Biology, 11 (2017), 1-12.
[16] S. Downes, The Success, Morphology, and Performance of Oxygenic Photogranules Under Light-Induced Stress Conditions, 2019.
[17] H. J. Eberl, D. F. Parker and M. C. Vanloosdrecht, A new deterministic spatio-temporal continuum model for biofilm development, Computational and Mathematical Methods in Medicine, 3 (2001), 161-175. · Zbl 0985.92009
[18] B. O. Emerenini, B. A. Hense, C. Kuttler and H. J. Eberl, A mathematical model of quorum sensing induced biofilm detachment, PloS one, 10 (2015).
[19] H. Feldman, X. Flores-Alsina, P. Ramin, K. Kjellberg, U. Jeppsson, D. J. Batstone and K. V. Gernaey, Modelling an industrial anaerobic granular reactor using a multi-scale approach, Water Research, 126 (2017), 488-500.
[20] H. C. Flemming and J. Wingender, The biofilm matrix, Nature Reviews Microbiology, 8 (2010), 623-633.
[21] H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice and S. Kjelleberg, Biofilms: An emergent form of bacterial life, Nature Reviews Microbiology, 14 (2016), 563-575.
[22] J. R. Flora, M. T. Suidan, P. Biswas and G. D. Sayles, Modeling algal biofilms: Role of carbon, light, cell surface charge, and ionic species, Water Environment Research, 67 (1995), 87-94.
[23] A. Friedman, Free boundary problems in biology, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 373 (2015), 16 pp. doi: 10.1098/rsta.2014.0368. · Zbl 1353.35291 · doi:10.1098/rsta.2014.0368
[24] A. Friedman, Free boundary problems for systems of stokes equations, Discrete Continuous Dynamical Systems-Series B, 21 (2016), 1455-1468. doi: 10.3934/dcdsb.2016006. · Zbl 1357.35298 · doi:10.3934/dcdsb.2016006
[25] W. Hao, L. S. Schlesinger and A. Friedman, Modeling granulomas in response to infection in the lung, PLoS One, 11 (2016).
[26] M. Heining and R. Buchholz, Photobioreactors with internal illumination-a survey and comparison, Biotechnology Journal, 10 (2015), 1131-1137.
[27] M. Heining, A. Sutor, S. C. Stute, C. P. Lindenberger and R. Buchholz, Internal illumination of photobioreactors via wireless light emitters: A proof of concept, Journal of Applied Phycology, 27 (2015), 59-66.
[28] A. Houry, M. Gohar, J. Deschamps, E. Tischenko, S. Aymerich, A. Gruss, Alexandra and R. Briandet, Bacterial swimmers that infiltrate and take over the biofilm matrix, Proceedings of the National Academy of Sciences, 109 (2012), 13088-13093.
[29] J. Hughes, H. J. Eberl and S. Sonner, A mathematical model of discrete attachment to a cellulolytic biofilm using random DEs, Mathematical Biosciences and Engineering, 19 (2022), 6582-6619. doi: 10.3934/mbe.2022310. · Zbl 1508.92155 · doi:10.3934/mbe.2022310
[30] D. Jones, H. V. Kojouharov, D. Le and H. Smith, The Freter model: A simple model of biofilm formation, Journal of Mathematical Biology, 47 (2003), 137-152. doi: 10.1007/s00285-003-0202-1. · Zbl 1023.92010 · doi:10.1007/s00285-003-0202-1
[31] J. C. Kissel, P. L. McCarty and R. L. Street, Numerical simulation of mixed-culture biofilm, Journal of Environmental Engineering, 110 (1984), 393-411.
[32] I. Klapper and B. Szomolay, An exclusion principle and the importance of mobility for a class of biofilm models, Bulletin of Mathematical Biology, 73 (2011), 2213-2230. doi: 10.1007/s11538-010-9621-5. · Zbl 1225.92057 · doi:10.1007/s11538-010-9621-5
[33] J. Kreft, C. Picioreanu, J. W. T. Wimpenny and C. M. van Loosdrecht, Individual-based modelling of biofilms, Microbiology, 147 (2001), 2897-2912.
[34] Y. Liu and J. H. Tay, The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge, Microbiology, 36 (2002), 1653-1665.
[35] A. Mašić and H. J. Eberl, Persistence in a single species CSTR model with suspended flocs and wall attached biofilms, Bulletin of Mathematical Biology, 74 (2012), 1001-1026. doi: 10.1007/s11538-011-9707-8. · Zbl 1235.92019 · doi:10.1007/s11538-011-9707-8
[36] A. Mašić and H. J. Eberl, A modeling and simulation study of the role of suspended microbial populations in nitrification in a biofilm reactor, Bulletin of Mathematical Biology, 76 (2014), 27-58. doi: 10.1007/s11538-013-9898-2. · Zbl 1283.92021 · doi:10.1007/s11538-013-9898-2
[37] M. R. Mattei, L. Frunzo, B. D’acunto, Y. Pechaud, F. Pirozzi and G. Esposito, Continuum and discrete approach in modeling biofilm development and structure: A review, Journal of Mathematical Biology, 76 (2018), 945-1003. doi: 10.1007/s00285-017-1165-y. · Zbl 1391.35378 · doi:10.1007/s00285-017-1165-y
[38] S. Mills, A. C. Trego, J. Ward, J. Castilla-Archilla, J. Hertel, I. Thiele, P. N. L. Lens, U. Z. Ijaz and G. Collins, Methanogenic granule growth and development is a continual process characterized by distinct morphological features, Journal of Environmental Management, 286 (2021), 112-229.
[39] J. Muñoz Sierra, C. Picioreanu and M. C. Van Loosdrecht, Modeling phototrophic biofilms in a plug-flow reactor, Water Science and Technology, 70 (2014), 1261-1270.
[40] M. Odriozola, I. López and L. Borzacconi, Modeling granule development and reactor performance on anaerobic granular sludge reactors, Journal of Environmental Chemical Engineering, 4 (2016), 1615-1628.
[41] J. Palmer, S. Flint and J. Brooks, Bacterial cell attachment, the beginning of a biofilm, Journal of Industrial Microbiology and Biotechnology, 34 (2007), 577-588.
[42] M. Plattes, E. Henry, P. M. Schosseler and A. Weidenhaupt, Modelling and dynamic simulation of a moving bed bioreactor for the treatment of municipal wastewater, Biochemical Engineering Journal, 32 (2006), 61-68.
[43] L. H. Pol, S. de Castro Lopes, G. Lettinga and P. N. Lens, Anaerobic sludge granulation, Water Research, 38 (2004), 1376-1389.
[44] G. Policastro, V. Luongo, L. Frunzo, N. Cogan and M. Fabbricino, A mechanistic mathematical model for photo fermentative hydrogen and polyhydroxybutyrate, Mathematical Biosciences and Engineering, 20 (2023), 7407-7428. doi: 10.3934/mbe.2023321. · doi:10.3934/mbe.2023321
[45] G. Policastro, V. Luongo, L. Frunzo and M. Fabbricino, A comprehensive review of mathematical models of photo fermentation, Critical Reviews in Biotechnology, 41 (2021), 628-648.
[46] K. A. Rahman, R. Sudarsan and H. J. Eberl, A mixed-culture biofilm model with cross-diffusion, Bulletin of Mathematical Biology, 77 (2015), 2086-2124. doi: 10.1007/s11538-015-0117-1. · Zbl 1339.92048 · doi:10.1007/s11538-015-0117-1
[47] Rodriguez, Carpio, Einarsson and others, A cellular automata model for biofilm growth, 10th World Congress on Computational Mechanics, Blucher Mechanical Engineering Proceedings, 1 (2014), 409-421.
[48] G. Roeselers, M. C. van Loosdrecht and G. Muyzer, Phototrophic biofilms and their potential applications, Journal of Applied Phycology, 20 (2008), 227-235.
[49] Y. Rohanizadegan, S. Sonner and H. J. Eberl, Discrete attachment to a cellulolytic biofilm modeled by an Itô stochastic differential equation, Mathematical Biosciences and Engineering, 17 (2020), 2236-2271. doi: 10.3934/mbe.2020119. · Zbl 1470.92199 · doi:10.3934/mbe.2020119
[50] Rumbaugh and Sauer, Biofilm dispersion, Nature Reviews Microbiology, 18 (2020), 571-586.
[51] F. Russo, V. Luongo, M. R. Mattei and L. Frunzo, Mathematical modeling of metal recovery from E-waste using a dark-fermentation-leaching process, Scientific Reports, 12 (2022).
[52] F. Russo, A. Tenore, M. R. Mattei and L. Frunzo, Multiscale modelling of the start-up process of anammox-based granular reactors, Mathematical Biosciences and Engineering, 19 (2022), 10374-10406. doi: 10.3934/mbe.2022486. · Zbl 1508.92158 · doi:10.3934/mbe.2022486
[53] J. Seok and S. J. Komisar, Integrated modeling of anaerobic fluidized bed bioreactor for deicing waste treatment. i: Model derivation, Journal of Environmental Engineering, 129 (2003), 100-109.
[54] Y. Tao and M. Chen, An elliptic-hyperbolic free boundary problem modelling cancer therapy, Nonlinearity, 19 (2006), 419-440. doi: 10.1088/0951-7715/19/2/010. · Zbl 1105.35149 · doi:10.1088/0951-7715/19/2/010
[55] A. Tenore, M. R. Mattei and L. Frunzo, Modelling oxygenic photogranules: Microbial ecology and process performance, SIAM Journal on Applied Mathematics, (2023), S362-S391. · Zbl 07906255
[56] A. Tenore, M. R. Mattei and L. Frunzo, Modelling the ecology of phototrophic-heterotrophic biofilms, Communications in Nonlinear Science and Numerical Simulation, 94 (2021). doi: 10.1016/j.cnsns.2020.105577. · Zbl 1455.35271 · doi:10.1016/j.cnsns.2020.105577
[57] A. Tenore, F. Russo, M. R. Mattei, B. D’Acunto, G. Collins and L. Frunzo, Multiscale modelling of de novo anaerobic granulation, Bulletin of Mathematical Biology, 83 (2021), 50 pp. doi: 10.1007/s11538-021-00951-y. · Zbl 1478.92124 · doi:10.1007/s11538-021-00951-y
[58] A. C. Trego, E. Galvin, C. Sweeney, S. Dunning, C. Murphy, S. Mills, C. Nzeteu, C. Quince, S. Connelly, U. Z. Ijaz, et al., Growth and break-up of methanogenic granules suggests mechanisms for biofilm and community development, Frontiers in Microbiology, 11 (2020).
[59] E. Volcke, C. Picioreanu, B. De Baets and M. C. Van Loosdrecht, Effect of granule size on autotrophic nitrogen removal in a granular sludge reactor, Environmental Technology, 31 (2010), 1271-1280.
[60] O. Wanner and W. Gujer, A multispecies biofilm model, Biotechnology and Bioengineering, 28 (1986), 314-328.
[61] G. Wolf, C. Picioreanu and M. C. van Loosdrecht, Kinetic modeling of phototrophic biofilms: The PHOBIA model, Biotechnology and Bioengineering, 97 (2007), 1064-1079.
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.