Please cite this article as: Carrel, M., Morales, Veró.L., Beltran, M.A., Derlon, N., Kaufmann, R., Morgenroth, E., Holzner, M., Biofilms in 3D porous media: Delineating the influence of the pore network geometry, flow and mass transfer on biofilm development, Water Research (2018Research ( ), doi: 10.1016Research ( / j.watres.2018 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. in the considered system, consistent with the excess supply of nutrient and electron acceptors. 50The wall shear stress remained constant in the vicinity of the biofilm but increased 51 substantially elsewhere.
Biofilms are ubiquitous bacterial communities that grow in various porous media including soils, trickling, and sand filters. In these environments, they play a central role in services ranging from degradation of pollutants to water purification. Biofilms dynamically change the pore structure of the medium through selective clogging of pores, a process known as bioclogging. This affects how solutes are transported and spread through the porous matrix, but the temporal changes to transport behavior during bioclogging are not well understood. To address this uncertainty, we experimentally study the hydrodynamic changes of a transparent 3‐D porous medium as it experiences progressive bioclogging. Statistical analyses of the system's hydrodynamics at four time points of bioclogging (0, 24, 36, and 48 h in the exponential growth phase) reveal exponential increases in both average and variance of the flow velocity, as well as its correlation length. Measurements for spreading, as mean‐squared displacements, are found to be non‐Fickian and more intensely superdiffusive with progressive bioclogging, indicating the formation of preferential flow pathways and stagnation zones. A gamma distribution describes well the Lagrangian velocity distributions and provides parameters that quantify changes to the flow, which evolves from a parallel pore arrangement under unclogged conditions, toward a more serial arrangement with increasing clogging. Exponentially evolving hydrodynamic metrics agree with an exponential bacterial growth phase and are used to parameterize a correlated continuous time random walk model with a stochastic velocity relaxation. The model accurately reproduces transport observations and can be used to resolve transport behavior at intermediate time points within the exponential growth phase considered.
X-ray tomography is a powerful tool giving access to the morphology of biofilms, in 3D porous media, at the mesoscale. Due to the high water content of biofilms, the attenuation coefficient of biofilms and water are very close, hindering the distinction between biofilms and water without the use of contrast agents. Until now, the use of contrast agents such as barium sulfate, silver-coated micro-particles or 1-chloronaphtalene added to the liquid phase allowed imaging the biofilm 3D morphology. However, these contrast agents are not passive and potentially interact with the biofilm when injected into the sample. Here, we use a natural inorganic compound, namely iron sulfate, as a contrast agent progressively bounded in dilute or colloidal form into the EPS matrix during biofilm growth. By combining a very long source-to-detector distance on a X-ray laboratory source with a Lorentzian filter implemented prior to tomographic reconstruction, we substantially increase the contrast between the biofilm and the surrounding liquid, which allows revealing the 3D biofilm morphology. A comparison of this new method with the method proposed by Davit et al (Davit et al., 2011), which uses barium sulfate as a contrast agent to mark the liquid phase was performed. Quantitative evaluations between the methods revealed substantial differences for the volumetric fractions obtained from both methods. Namely, contrast agent—biofilm interactions (e.g. biofilm detachment) occurring during barium sulfate injection caused a reduction of the biofilm volumetric fraction of more than 50% and displacement of biofilm patches elsewhere in the column. Two key advantages of the newly proposed method are that passive addition of iron sulfate maintains the integrity of the biofilm prior to imaging, and that the biofilm itself is marked by the contrast agent, rather than the liquid phase as in other available methods. The iron sulfate method presented can be applied to understand biofilm development and bioclogging mechanisms in porous materials and the obtained biofilm morphology could be an ideal basis for 3D numerical calculations of hydrodynamic conditions to investigate biofilm-flow coupling.
Bacterial biofilms can form in porous media that are of interest in industrial applications ranging from medical implants to biofilters as well as in environmental applications such as in situ groundwater remediation, where they can be critical locations for biogeochemical reactions. The presence of biofilms modifies porous media topology and hydrodynamics by clogging pores and consequently solutes transport and reactions kinetics. The interplay between highly heterogeneous flow fields found in porous media and microbial behavior, including biofilm growth, results in a spatially heterogeneous biofilm distribution in the porous media as well as internal heterogeneity across the thickness of the biofilm. Our study leverages highly resolved three-dimensional X-ray computed microtomography images of bacterial biofilms in a tubular reactor to numerically compute pore-scale fluid flow and solute transport by considering multiple equivalent stochastically generated internal permeability fields for the biofilm. We show that the internal heterogeneous permeability mainly impacts intermediate velocities when compared with homogeneous biofilm permeability. While the equivalent internal permeability fields of the biofilm do not impact fluid–fluid mixing, they significantly control a fast reaction. For biologically driven reactions such as nutrient or contaminant uptake by the biofilm, its internal permeability field controls the efficiency of the process. This study highlights the importance of considering the internal heterogeneity of biofilms to better predict reactivity in industrial and environmental bioclogged porous systems.
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