Modeling Substrate Utilization, Metabolite Production, and Uranium Immobilization in Shewanella oneidensis Biofilms
Open Access
- 29 June 2017
- journal article
- research article
- Published by Frontiers Media SA in Frontiers in Environmental Science
Abstract
In this study, we developed a two-dimensional mathematical model to predict substrate utilization and metabolite production rates in Shewanella oneidensis MR-1 biofilm in the presence and absence of uranium (U). In our model, lactate and fumarate are used as the electron donor and the electron acceptor, respectively. The model includes the production of extracellular polymeric substances (EPS). The EPS bound to the cell surface and distributed in the biofilm were considered bound EPS (bEPS) and loosely associated EPS (laEPS), respectively. COMSOL® Multiphysics finite element analysis software was used to solve the model numerically (model file provided in the Supplementary Material). The input variables of the model were the lactate, fumarate, cell and EPS concentrations, half saturation constant for fumarate, and diffusion coefficients of the substrates and metabolites. To estimate unknown parameters and calibrate the model, we used a custom designed biofilm reactor placed inside a nuclear magnetic resonance (NMR) microimaging and spectroscopy system and measured substrate utilization and metabolite production rates. From these data we estimated the yield coefficients, maximum substrate utilization rate, half saturation constant for lactate, stoichiometric ratio of fumarate and acetate to lactate and stoichiometric ratio of succinate to fumarate. These parameters are critical to predicting the activity of biofilms and are not available in the literature. Lastly, the model was used to predict uranium immobilization in S. oneidensis MR-1 biofilms by considering reduction and adsorption processes in the cells and in the EPS. We found that the majority of immobilization was due to cells, and that EPS was less efficient at immobilizing U. Furthermore, most of the immobilization occurred within the top 10 μm of the biofilm. To the best of our knowledge, this research is one of the first biofilm immobilization mathematical models based on experimental observation. It has the ability to predict the relative contributions to U immobilization of laEPS, bEPS, and cells.Keywords
This publication has 65 references indexed in Scilit:
- Enhanced Uranium Immobilization and Reduction by Geobacter sulfurreducens BiofilmsApplied and Environmental Microbiology, 2014
- Biofilm shows spatially stratified metabolic responses to contaminant exposureEnvironmental Microbiology, 2012
- Contribution of Extracellular Polymeric Substances from Shewanella sp. HRCR-1 Biofilms to U(VI) ImmobilizationEnvironmental Science & Technology, 2011
- Extracellular polymeric substances from Shewanella sp. HRCR‐1 biofilms: characterization by infrared spectroscopy and proteomicsEnvironmental Microbiology, 2011
- Uranium Immobilization by Sulfate-Reducing BiofilmsEnvironmental Science & Technology, 2004
- MICROBIAL BIOFILMSAnnual Review of Microbiology, 1995
- Direct detection of trace levels of uranium by laser-induced kinetic phosphorimetryAnalytical Chemistry, 1992
- Analysis of double‐substrate limited growthBiotechnology & Bioengineering, 1978
- Accelerating diffusion with mixed solventsAIChE Journal, 1972
- Application of the Theory of Diffusion-controlled Reactions to Enzyme KineticsThe Journal of Physical Chemistry, 1958