Effects of aqueous uranyl speciation on the kinetics of microbial uranium reduction

Abstract

The ability to predict the success of the microbial reduction of soluble U(VI) to highly insoluble U(IV) as an in situ bioremediation strategy is complicated by the wide range of geochemical conditions at contaminated sites and the strong influence of aqueous uranyl speciation on the bioavailability and toxicity of U(VI) to metal-reducing bacteria. To determine the effects of aqueous uranyl speciation on uranium bioreduction kinetics, incubations and viability assays with Shewanella putrefaciens strain 200 were conducted over a range of pH and dissolved inorganic carbon (DIC), Ca 2+ , and Mg 2+ concentrations. A speciation-dependent kinetic model was developed to reproduce the observed time series of total dissolved uranium concentration over the range of geochemical conditions tested. The kinetic model yielded the highest rate constant for the reduction of uranyl non-carbonate species (i.e., the 'free' hydrated uranyl ion, uranyl hydroxides, and other minor uranyl complexes), indicating that they represent the most readily reducible fraction of U(VI) despite being the least abundant uranyl species in solution. The presence of DIC, Ca 2+ , and Mg 2+ suppressed the formation of more bioavailable uranyl non-carbonate species and resulted in slower bioreduction rates. At high concentrations of bioavailable U(VI), however, uranium toxicity to S. putrefaciens inhibited bioreduction, and viability assays confirmed that the concentration of non-carbonate uranyl species best predicts the degree of toxicity. The effect of uranium toxicity was accounted for by incorporating the free ion activity model of metal toxicity into the bioreduction rate law. Overall, these results demonstrate that, in the absence of competing terminal electron acceptors, uranium bioreduction kinetics can be predicted over a wide range of geochemical conditions based on the bioavailability and toxicity imparted on U(VI) by solution composition. These findings also imply that the concentration of uranyl non-carbonate species, despite being extremely low, is a determining factor controlling uranium bioreduction at contaminated sites.

Interaction of Uranium with Bacterial Cell Surfaces: Inferences from Phosphatase-Mediated Uranium Precipitation

“…It is important to understand how these different U species interact with bacterial cellular surfaces, especially for designing biological wastewater treatment systems. However, studies evaluating the effect of aqueous U speciation have been largely limited to biosorption, bioaccumulation, and bioreduction (9,15,16,20).…”

“…U forms aqueous species as a result of complexation with ligands under different pH conditions (14). In open atmospheric systems, under oxygenic conditions, and with pH values lower than 3, U(VI) is present exclusively in the form of hexavalent uranyl cation, UO 2 2ϩ , which is the most bioavailable form of U (15,16 predominate (17-19). It is important to understand how these different U species interact with bacterial cellular surfaces, especially for designing biological wastewater treatment systems.…”

“…It is important to understand how these different U species interact with bacterial cellular surfaces, especially for designing biological wastewater treatment systems. However, studies evaluating the effect of aqueous U speciation have been largely limited to biosorption, bioaccumulation, and bioreduction (9,15,16,20).Among the biological mechanisms involved in metal remediation, enzymatic bioprecipitation of heavy metals as metal phosphates is particularly attractive and is considered to be a promising approach for biological treatment of U effluents due to its high efficiency (14, 21). Bioprecipitation of metals as phosphates is mediated by phosphatases that cleave a phosphomonoester substrate (such as ␤-glycerophosphate) to release the phosphate moiety, which in turn precipitates heavy metals, such as U, Cd, Ni, Am, etc., from solutions (22, 23).…”

pH‐dependent speciation and hydrogen (H2) control U(VI) respiration by Desulfovibrio vulgaris

“…Cytochrome c3 has a mid-point redox potential near −300 mV versus SHE (standard hydrogen electrode) at 25°C (Niki et al, 1984), while the U(VI)-U(IV) couple has a mid-point potential of +334 mV versus SHE of dissolved inorganic carbon (DIC) and with a wide range of pH is of paramount importance for understanding microbial reduction of U(VI), since different U(VI) species could have different susceptibilities of being reduced based on their bioavailability. A decrease in U(VI) reduction rate with increasing DIC concentration, along with sensitivity towards pH, has been well documented in the literature (Belli et al, 2015;Bernhard, Geipel, Brendler, & Nitsche, 1998;Brooks et al, 2003;Croteau, Fuller, Cain, Campbell, & Aiken, 2016;Drobot et al, 2015;Guillauont et al, 2003;Jones et al, 2015;Sheng & Fein, 2014;Ulrich et al, 2011).…”

“…Carbonate is a key ligand in natural environments, and it influences the speciation of uranium (Clark, Hobart, & Neu, 1995;Langmuir, 1978;Stumm & Morgan, 1996), along with being an important pH buffer. Although U(VI) speciation and bioavailability of U(VI) in its different complexes have been studied for decades in isolation (Belli, DiChristina, Cappellen, & Taillefert, 2015;Brooks et al, 2003;Murphy & Shock, 1999;Stewart, Amos, Nico, & Fendorf, 2011;Sheng & Fein, 2014;Ulrich, Veeramani, Latmani, & Giammar, 2011), the connections between aqueous uranyl speciation, and electron partitioning between respiration & fermentation during U(VI) bioreduction were seldom studied. In sulfate-reducing conditions, the availability of the electron acceptor affects how electrons from the electron donor (lactate in our case) are distributed among fermentation and respiration end products.…”