Biogeochemical Controls on the Product of Microbial U(VI) Reduction

Abstract

Biologically mediated immobilization of radionuclides in the subsurface is a promising strategy for the remediation of uranium-contaminated sites. During this process, soluble U(VI) is reduced by indigenous microorganisms to sparingly soluble U(IV). The crystalline U(IV) phase uraninite, or UO 2 , is the preferable end-product of bioremediation due to its relatively high stability and low solubility in comparison to biomass-associated nonuraninite U(IV) species that have been reported in laboratory and under field conditions. The goal of this study was to delineate the geochemical conditions that promote the formation of nonuraninite U(IV) versus uraninite and to decipher the mechanisms of its preferential formation. U(IV) products were prepared under varying geochemical conditions and characterized with X-ray absorption spectroscopy (XAS), scanning transmission X-ray microscopy (STXM), and various wet chemical methods. We report an increasing fraction of nonuraninite U(IV) species with decreasing initial U concentration. Additionally, the presence of several common groundwater solutes (sulfate, silicate, and phosphate) promote the formation of nonuraninite U(IV). Our experiments revealed that the presence of those solutes promotes the formation of bacterial extracellular polymeric substances (EPS) and increases bacterial viability, suggesting that the formation of nonuraninite U(IV) is due to a biological response to solute presence during U(VI) reduction. The results obtained from this laboratory-scale research provide insight into biogeochemical controls on the product(s) of uranium reduction during bioremediation of the subsurface.

Mechanism of Uranium Reduction and Immobilization in Desulfovibrio vulgaris Biofilms

“…The presence of the microbial biofilm favored the formation of noncrystalline U(IV) by binding U(IV) within the biofilm matrix, and by this, precluding the precipitation of uraninite. This finding confirms the results presented previously 15 that correlated the formation of noncrystalline U(IV) with the presence of bacterial EPS. Moreover, noncrystalline U(IV) species were shown to be associated with cell-bound phosphate groups pointing to the involvement of bacterial phospholipids (one of the components of EPS).…”

The product of microbial uranium reduction includes multiple species with U(IV)–phosphate coordination

“…Because the FTIR analysis is sensitive to changes in the relative intensity of the amide I and II bands, it is also possible to detect a clear signal for a shift in protein composition as a result of the presence of U. This finding echoes previous transcriptomic work ( BencheikhLatmani et al, 2005) and suggests a toxicity response of S. oneidensis cells to U that includes increased production of phosphate-rich EPS that contains binding sites for U(IV) Stylo et al, 2013). Our work points to the simultaneous formation of a spectrum of U(IV)-containing species, including fractions of biogenic uraninite as determined by combined U EXAFS analyses and bicarbonate extractions (Alessi et al, 2012), noncrystalline U(IV) species that occur as phosphate coordination polymers or biomass-associated monomers, and U(IV)-phosphate precipitates such as ningyoite (Bernier-Latmani et al, 2010;Rui et al, 2013).…”

“…Due to the relatively higher lability of noncrystalline U(IV) (Alessi et al, 2012), unraveling its structure is critical to providing some understanding of conditions promoting its formation. Previous studies have established that the ratio of uraninite to noncrystalline U(IV) formed is strongly impacted by the ions present in the reduction solution or medium (Bernier-Latmani et al, 2010;Boyanov et al, 2011;Stylo et al, 2013) and have hypothesized that noncrystalline U(IV) species were coordinated to phosphate by inferring the possibility from fitting of U L III -edge EXAFS spectra and evidence of U(IV) and P co-occurrence from elemental mapping during electron microscopy analyses (Bernier-Latmani et al, 2010). Here, using combined spectroscopy and wet chemical techniques, we have demonstrated unambiguously that noncrystalline U(IV) is comprised of multiple U(IV) species bonded to phosphate groups.…”

“…Recent studies show that EPS contains a mixture of phosphate-bearing organic molecules and polymers such as nucleic acids, proteins, lipids, and polysaccharides (Flemming et al, 2007;Flemming and Wingender, 2010;McCrate et al, 2013). Stylo et al (2013) demonstrated that during uranium reduction, cells in medium containing some anions (e.g., phosphate, sulfate) produce more EPS than those in medium devoid of these solutes, likely because they are required for the cells to be in a viable physiological state. Transmission electron microscopy (TEM) analyses, conducted on microbial U(VI) reduction samples identical to those studied here, indicated a spatial correlation between extracellular U and P (Bernier-Latmani et al, 2010).…”

Calcification and Diagenesis of Bacterial Colonies

“…The highly structured sub-micrometric association of calcite with organic molecules dominated by proteic moieties exhibited by the contemporary bacterial colonies suggests a formation resulting from biomineralization processes [60,70]. Two main pathways of bacteria-induced/controlled carbonate precipitation have been reported in modern environments and laboratory cultures [64,[71][72][73][74].…”