Contribution of Extracellular Polymeric Substances from Shewanella sp. HRCR-1 Biofilms to U(VI) Immobilization

Safe and effective nuclear waste disposal, as well as accidental radionuclide releases, necessitates our understanding of the fate of radionuclides in the environment, including their interaction with microorganisms. We examined the sorption of Pu(IV) and Pu(V) to Pseudomonas sp. strain EPS-1W, an aerobic bacterium isolated from plutonium (Pu)-contaminated groundwater collected in the United States at the Nevada National Security Site (NNSS) in Nevada. We compared Pu sorption to cells with and without bound extracellular polymeric substances (EPS). Wild-type cells with intact EPS sorbed Pu(V) more effectively than cells with EPS removed. In contrast, cells with and without EPS showed the same sorption affinity for Pu(IV). In vitro experiments with extracted EPS revealed rapid reduction of Pu(V) to Pu(IV). Transmission electron microscopy indicated that 2-to 3-nm nanocrystalline Pu(IV)O 2 formed on cells equilibrated with high concentrations of Pu(IV) but not Pu(V). Thus, EPS, while facilitating Pu(V) reduction, inhibit the formation of nanocrystalline Pu(IV) precipitates. IMPORTANCEOur results indicate that EPS are an effective reductant for Pu(V) and sorbent for Pu(IV) and may impact Pu redox cycling and mobility in the environment. Additionally, the resulting Pu morphology associated with EPS will depend on the concentration and initial Pu oxidation state. While our results are not directly applicable to the Pu transport situation at the NNSS, the results suggest that, in general, stationary microorganisms and biofilms will tend to limit the migration of Pu and provide an important Pu retardation mechanism in the environment. In a broader sense, our results, along with a growing body of literature, highlight the important role of microorganisms as producers of redox-active organic ligands and therefore as modulators of radionuclide redox transformations and complexation in the subsurface.T he civil production of nuclear energy and military production of nuclear materials have resulted in an estimated worldwide inventory of over 2,000 metric tons of plutonium (Pu) (1). This inventory continues to increase at a rate of approximately 70 metric tons per year as a result of global nuclear energy production (2). Due to its long half-life (24,100 years for 239 Pu) and high radiotoxicity (3), Pu is an important driver in public health risk assessments for nuclear waste repositories and radiologically contaminated sites. However, predicting how Pu behaves in the environment and ultimately calculating its human health risk are limited by our understanding of the dominant biogeochemical processes controlling its behavior.The behavior of Pu in the environment is strongly dependent on its oxidation state and concentration. Among all the actinides, Pu has one of the most complex chemical, redox, and surface sorption behaviors. At low concentrations, Pu can exist as aqueous species in the III, IV, V, and/or VI oxidation states, all of which have different solubilities (4), mineral sorption affinities (5-7), and hence...

Section: Discussionsupporting

confidence: 87%

“…Previous research demonstrates that EPS of bacterial origin are able to interact with metals, including actinides such as uranium and neptunium, and alter their redox and solubility properties (29)(30)(31)(32). However, to the best of our knowledge, no studies on the specific interaction of Pu with EPS have been reported under oxic conditions.…”

mentioning

confidence: 98%

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Boggs

Jiao

Dai

et al. 2016

“…However, the contribution of Geobacter biofilms to these processes and their potential use as bioremediation tools have not been fully investigated. This contrasts with the availability of studies about U transformations mediated by Geobacter planktonic cells (14,15,23,28,29) or by biofilms formed by other metal-reducing bacteria, such as Desulfovibrio (30,31) and Shewanella (32,33). Hence, we investigated U transformations mediated by biofilms of G. sulfurreducens.…”

mentioning

confidence: 95%

Enhanced Uranium Immobilization and Reduction by Geobacter sulfurreducens Biofilms

Cologgi

Speers

Bullard

et al. 2014

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.

“…Biofilms of S. oneidensis play an important role in many environmental and biotechnological processes, including removing toxic metal contaminants, such as uranium and chromium, from the aqueous phase by transforming them into less soluble species (17,(19)(20)(21). Previous studies have suggested that exposure to toxic contaminants, e.g., chromate, could cause dispersal of S. oneidensis biofilms (14).…”

mentioning

confidence: 99%

Disruption of Putrescine Biosynthesis in Shewanella oneidensis Enhances Biofilm Cohesiveness and Performance in Cr(VI) Immobilization

Ding

Peng

et al. 2014

Self Cite

121

159

Although biofilm-based bioprocesses have been increasingly used in various applications, the long-term robust and efficient biofilm performance remains one of the main bottlenecks. In this study, we demonstrated that biofilm cohesiveness and performance of Shewanella oneidensis can be enhanced through disrupting putrescine biosynthesis. Through random transposon mutagenesis library screening, one hyperadherent mutant strain, CP2-1-S1, exhibiting an enhanced capability in biofilm formation, was obtained. Comparative analysis of the performance of biofilms formed by S. oneidensis MR-1 wild type (WT) and CP2-1-S1 in removing dichromate (Cr 2 O 7 2؊ ), i.e., Cr(VI), from the aqueous phase showed that, compared with the WT biofilms, CP2-1-S1 biofilms displayed a substantially lower rate of cell detachment upon exposure to Cr(VI), suggesting a higher cohesiveness of the mutant biofilms. In addition, the amount of Cr(III) immobilized by CP2-1-S1 biofilms was much larger, indicating an enhanced performance in Cr(VI) bioremediation. We further showed that speF, a putrescine biosynthesis gene, was disrupted in CP2-1-S1 and that the biofilm phenotypes could be restored by both genetic and chemical complementations. Our results also demonstrated an important role of putrescine in mediating matrix disassembly in S. oneidensis biofilms.