Enhanced Uranium Immobilization and Reduction by Geobacter sulfurreducens Biofilms

Abstract

Biofilms formed by dissimilatory metal reducers are of interest to develop permeable biobarriers for the immobilization of soluble contaminants such as uranium. Here we show that biofilms of the model uranium-reducing bacterium Geobacter sulfurreducens immobilized substantially more U(VI) than planktonic cells and did so for longer periods of time, reductively precipitating it to a mononuclear U(IV) phase involving carbon ligands. The biofilms also tolerated high and otherwise toxic concentrations (up to 5 mM) of uranium, consistent with a respiratory strategy that also protected the cells from uranium toxicity. The enhanced ability of the biofilms to immobilize uranium correlated only partially with the biofilm biomass and thickness and depended greatly on the area of the biofilm exposed to the soluble contaminant. In contrast, uranium reduction depended on the expression of Geobacter conductive pili and, to a lesser extent, on the presence of the c cytochrome OmcZ in the biofilm matrix. The results support a model in which the electroactive biofilm matrix immobilizes and reduces the uranium in the top stratum. This mechanism prevents the permeation and mineralization of uranium in the cell envelope, thereby preserving essential cellular functions and enhancing the catalytic capacity of Geobacter cells to reduce uranium. Hence, the biofilms provide cells with a physically and chemically protected environment for the sustained immobilization and reduction of uranium that is of interest for the development of improved strategies for the in situ bioremediation of environments impacted by uranium contamination.

Modeling Substrate Utilization, Metabolite Production, and Uranium Immobilization in Shewanella oneidensis Biofilms

“…In our model, the majority of uranium present within the biofilm was reduced rather than sorbed. This is similar to results for another dissimilatory metal-reducing bacteria capable of reducing U, Geobacter sulfurreducens (Renslow R. S. et al, 2013;Cologgi et al, 2014). Cologgi et al (2014) demonstrated that biofilms and EPS provide cells with a physically and chemically protected environment, which is at least partially due to restricted transport of potentially harmful compounds.…”

“…This is similar to results for another dissimilatory metal-reducing bacteria capable of reducing U, Geobacter sulfurreducens (Renslow R. S. et al, 2013;Cologgi et al, 2014). Cologgi et al (2014) demonstrated that biofilms and EPS provide cells with a physically and chemically protected environment, which is at least partially due to restricted transport of potentially harmful compounds. In conclusion, U did not dramatically affect overall cell growth or metabolism in biofilms, largely because U did not penetrate very far into the biofilm, indicating the protective ability of the biofilm.…”

Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis

“…Understanding the metabolic fate of uranyl species in bacterial communities is a prerequisite to designing bioremediation strategies that are based on naturally occurring detoxification mechanisms (9,10). The impact of other redoxactive heavy metals, such as copper or iron, on cell physiology has often been related to their ability to catalyze Fenton-type reactions, leading to hydroxyl radical formation and consequently to cell damage by the formation of other reactive oxygen species (ROS).…”

Harnessing the power of microbial nanowires

“…Genetic manipulation of the number of T4P produced per cell or their rates of charge transport could effectively alleviate the electron acceptor limitation imposed by the accumulation of reduced c‐Cyts in the top layers of thick biofilms and improve the performance of bioanodes. In addition to stacking more cells on electrodes, the GS pili and, to a lesser extent, matrix‐associated c‐Cyts, enhance the capacity of cells in biofilms to bind and reduce soluble, toxic metals such as the uranyl cation (Cologgi et al ., 2014), a catalytic activity that could be harnessed to develop permeable biobarriers for the in‐situ bioremediation of metal contaminants.…”