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.
Highlights
Microorganisms interact with minerals available in the environment (Zhou et al, 2014; Ng et al, 2016; Shi et al, 2016)
The parameters derived from the experimental data and the values from the literature were not significantly different from each other, except the fAc/ED value, which was significantly lower than the value obtained from a similar experiment by Cao et al (2012) (Table 3)
The maximum specific growth rate calculated from the model cell yield and maximum specific substrate utilization rate was 0.08 h−1, which is close to the reported value of 0.087–0.125 h−1 (Tang et al, 2007a; Hunt et al, 2010)
Summary
Microorganisms interact with minerals available in the environment (Zhou et al, 2014; Ng et al, 2016; Shi et al, 2016). Shewanella oneidensis MR-1 is one type of dissimilatory metal-reducing bacterium that plays an important role in the biogeochemical cycling of many different types of metals and radionuclides (Venkateswaran et al, 1999; Nealson et al, 2002; Marshall et al, 2006; Nealson and Scott, 2006) This organism is capable of utilizing a wide range of electron donors, such as lactate, acetate, pyruvate, formate, and amino acids, and electron acceptors, such as oxygen (O2), fumarate, dimethyl sulfoxide (DMSO), Fe(III), and Mn(IV) (Myers and Nealson, 1988; Nealson and Saffarini, 1994; Tang et al, 2007b; Mclean et al, 2008a; Pinchuk et al, 2011). Since the biotransformation of metals and radionuclides (e.g., during uranium bioremediation) can impact cellular metabolism (Viamajala et al, 2002, 2004; Tang et al, 2006), it is important to investigate experimentally and theoretically using mathematical models, and understand these changes in order to improve bioremediation techniques and applications
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