Kate M. Campbell

Biogeochemical Redox Processes and their Impact on Contaminant Dynamics

Life and element cycling on Earth is directly related to electron transfer (or redox) reactions. An understanding of biogeochemical redox processes is crucial for predicting and protecting environmental health and can provide new opportunities for engineered remediation strategies. Energy can be released and stored by means of redox reactions via the oxidation of labile organic carbon or inorganic compounds (electron donors) by microorganisms coupled to the reduction of electron acceptors including humic substances, iron-bearing minerals, transition metals, metalloids, and actinides. Environmental redox processes play key roles in the formation and dissolution of mineral phases. Redox cycling of naturally occurring trace elements and their host minerals often controls the release or sequestration of inorganic contaminants. Redox processes control the chemical speciation, bioavailability, toxicity, and mobility of many major and trace elements including Fe, Mn, C, P, N, S, Cr, Cu, Co, As, Sb, Se, Hg, Tc, and U. Redox-active humic substances and mineral surfaces can catalyze the redox transformation and degradation of organic contaminants. In this review article, we highlight recent advances in our understanding of biogeochemical redox processes and their impact on contaminant fate and transport, including future research needs.

Uranium redox transition pathways in acetate-amended sediments

Redox transitions of uranium [from U(VI) to U(IV)] in low-temperature sediments govern the mobility of uranium in the environment and the accumulation of uranium in ore bodies, and inform our understanding of Earth’s geochemical history. The molecular-scale mechanistic pathways of these transitions determine the U(IV) products formed, thus influencing uranium isotope fractionation, reoxidation, and transport in sediments. Studies that improve our understanding of these pathways have the potential to substantially advance process understanding across a number of earth sciences disciplines. Detailed mechanistic information regarding uranium redox transitions in field sediments is largely nonexistent, owing to the difficulty of directly observing molecular-scale processes in the subsurface and the compositional/physical complexity of subsurface systems. Here, we present results from an in situ study of uranium redox transitions occurring in aquifer sediments under sulfate-reducing conditions. Based on molecular-scale spectroscopic, pore-scale geochemical, and macroscale aqueous evidence, we propose a biotic–abiotic transition pathway in which biomass-hosted mackinawite (FeS) is an electron source to reduce U(VI) to U(IV), which subsequently reacts with biomass to produce monomeric U(IV) species. A species resembling nanoscale uraninite is also present, implying the operation of at least two redox transition pathways. The presence of multiple pathways in low-temperature sediments unifies apparently contrasting prior observations and helps to explain sustained uranium reduction under disparate biogeochemical conditions. These findings have direct implications for our understanding of uranium bioremediation, ore formation, and global geochemical processes.

Oxidative Dissolution of Biogenic Uraninite in Groundwater at Old Rifle, CO

Reductive bioremediation is currently being explored as a possible strategy for uranium-contaminated aquifers such as the Old Rifle site (Colorado). The stability of U(IV) phases under oxidizing conditions is key to the performance of this procedure. An in situ method was developed to study oxidative dissolution of biogenic uraninite (UO₂), a desirable U(VI) bioreduction product, in the Old Rifle, CO, aquifer under different variable oxygen conditions. Overall uranium loss rates were 50-100 times slower than laboratory rates. After accounting for molecular diffusion through the sample holders, a reactive transport model using laboratory dissolution rates was able to predict overall uranium loss. The presence of biomass further retarded diffusion and oxidation rates. These results confirm the importance of diffusion in controlling in-aquifer U(IV) oxidation rates. Upon retrieval, uraninite was found to be free of U(VI), indicating dissolution occurred via oxidation and removal of surface atoms. Interaction of groundwater solutes such as Ca²⁺ or silicate with uraninite surfaces also may retard in-aquifer U loss rates. These results indicate that the prolonged stability of U(IV) species in aquifers is strongly influenced by permeability, the presence of bacterial cells and cell exudates, and groundwater geochemistry.

Surface Complexation Modeling of U(VI) Adsorption by Aquifer Sediments from a Former Mill Tailings Site at Rifle, Colorado

A study of U(VI) adsorption by aquifer sediment samples from a former uranium mill tailings site at Rifle, Colorado, was conducted under oxic conditions as a function of pH, U(VI), Ca, and dissolved carbonate concentration. Batch adsorption experiments were performed using <2 mm size sediment fractions, a sand-sized fraction, and artificial groundwater solutions prepared to simulate the field groundwater composition. To encompass the geochemical conditions of the alluvial aquifer at the site, the experimental conditions ranged from 6.8 x 10(-8) to 10(-5) M in [U(VI)](tot), 7.2 to 8.0 in pH, 3.0 x 10(-3) to 6.0 x 10(-3) M in [Ca(2+)], and 0.05 to 2.6% in partial pressure of carbon dioxide. Surface area normalized U(VI) adsorption K(d) values for the sand and <2 mm sediment fraction were similar, suggesting a similar reactive surface coating on both fractions. A two-site two-reaction, nonelectrostatic generalized composite surface complexation model was developed and successfully simulated the U(VI) adsorption data. The model successfully predicted U(VI) adsorption observed from a multilevel sampling well installed at the site. A comparison of the model with the one developed previously for a uranium mill tailings site at Naturita, Colorado, indicated that possible calcite nonequilibrium of dissolved calcium concentration should be evaluated. The modeling results also illustrate the importance of the range of data used in deriving the best fit model parameters.

Rate‐limited U(VI) desorption during a small‐scale tracer test in a heterogeneous uranium‐contaminated aquifer

[1] A tracer test was performed at the Rifle Integrated Field Research Challenge site to assess the effect of addition of bicarbonate on U(VI) desorption from contaminated sediments in the aquifer and to compare equilibrium and rate-limited reactive transport model descriptions of mass transfer limitations on desorption. The tracer test consisted of injection of a 37 mM NaHCO3 solution containing conservative tracers followed by downgradient sampling of groundwater at various elevations and distances from the point of injection. Breakthrough curves show that dissolved U(VI) concentrations increased 1.2–2.6-fold above background levels, resulting from increases in bicarbonate alkalinity (from injectate solution) and Ca concentrations (from cation exchange). In general, more U(VI) was mobilized in shallower zones of the aquifer, where finer-grained sediments and higher solid phase U content were found compared to deeper zones. An equilibrium-based reactive transport model incorporating a laboratory-based surface complexation model derived from the same location predicted the general trends in dissolved U(VI) during the tracer test but greatly overpredicted the concentrations of U(VI), indicating that the system was not at equilibrium. Inclusion of a multirate mass transfer model successfully simulated the nonequilibrium desorption behavior of U(VI). Local sediment properties such as sediment texture (weight percent <2 mm), surface area, cation exchange capacity, and adsorbed U(VI) were heterogeneous at the meter scale, and it was important to incorporate these values into model parameters in order to produce accurate simulations.

Evaluating Chemical Extraction Techniques for the Determination of Uranium Oxidation State in Reduced Aquifer Sediments

Extraction techniques utilizing high pH and (bi)carbonate concentrations were evaluated for their efficacy in determining the oxidation state of uranium (U) in reduced sediments collected from Rifle, CO. Differences in dissolved concentrations between oxic and anoxic extractions have been proposed as a means to quantify the U(VI) and U(IV) content of sediments. An additional step was added to anoxic extractions using a strong anion exchange resin to separate dissolved U(IV) and U(VI). X-ray spectroscopy showed that U(IV) in the sediments was present as polymerized precipitates similar to uraninite and/or less ordered U(IV), referred to as non-uraninite U(IV) species associated with biomass (NUSAB). Extractions of sediment containing both uraninite and NUSAB displayed higher dissolved uranium concentrations under oxic than anoxic conditions while extractions of sediment dominated by NUSAB resulted in identical dissolved U concentrations. Dissolved U(IV) was rapidly oxidized under anoxic conditions in all experiments. Uraninite reacted minimally under anoxic conditions but thermodynamic calculations show that its propensity to oxidize is sensitive to solution chemistry and sediment mineralogy. A universal method for quantification of U(IV) and U(VI) in sediments has not yet been developed but the chemical extractions, when combined with solid-phase characterization, have a narrow range of applicability for sediments without U(VI).

Biogenic non-crystalline U (IV) revealed as major component in uranium ore deposits

Historically, it is believed that crystalline uraninite, produced via the abiotic reduction of hexavalent uranium (U(VI)) is the dominant reduced U species formed in low-temperature uranium roll-front ore deposits. Here we show that non-crystalline U(IV) generated through biologically mediated U(VI) reduction is the predominant U(IV) species in an undisturbed U roll-front ore deposit in Wyoming, USA. Characterization of U species revealed that the majority (∼58-89%) of U is bound as U(IV) to C-containing organic functional groups or inorganic carbonate, while uraninite and U(VI) represent only minor components. The uranium deposit exhibited mostly 238U-enriched isotope signatures, consistent with largely biotic reduction of U(VI) to U(IV). This finding implies that biogenic processes are more important to uranium ore genesis than previously understood. The predominance of a relatively labile form of U(IV) also provides an opportunity for a more economical and environmentally benign mining process, as well as the design of more effective post-mining restoration strategies and human health-risk assessment.

How electron flow controls contaminant dynamics.

Anthropogenic and natural sources of pollution contribute large amounts of inorganic and organic compounds to the global environment every day. As a result, public health issues and ecosystem deterioration arising from environmental pollution are growing concerns worldwide. Ecosystem services are influenced by intimately coupled relationships between humans and the biological, chemical, and physical characteristics of our natural environment. The rapid growth in the global population and the increasing pressure of understanding and addressing the sustainability of air, soil, and water resources in response to global change and human activities will require transdisciplinary research efforts resulting in the development of science-based solution strategies. The interfaces between oxic and anoxic environments are often of particular importance for element cycling and the fate of contaminants. Such environments include shallow aquifers, river floodplains, rice paddy soils, wetlands, thawing permafrost soils, hydrothermal hot springs, lake sediments, and many others. These environments are true “hotspots” of biogeochemical activity that control element cycles. The redox cycling of organic carbon and nitrogen not only drive the microand macro-biological communities, but also have implications for global nutrient balances and climate change. For example, methane emission from wetlands, rice paddies, and thawing permafrost soils contributes significantly to the overall greenhouse gas budget on Earth. Riparian floodplain soils can act either as sinks or sources of nutrients and contaminants, and important contaminant transformations take place in such environments (e.g., Hg-methylation, sulfide formation, or sulfide oxidation). Biogeochemical redox processes occurring in these environments play a key role in controlling the behavior of inorganic and organic contaminants. For example, bacteria can reduce or oxidize many metals (e.g., Fe, Mn, Cu, Hg), metalloids (e.g., As), and nonmetals (e.g., Se) with important consequences for their chemical speciation, mobility, and toxicity. Similarly, the migration behavior of radionuclides (e.g., U, Pu) is often directly affected by abiotic or biotic redox processes. Biogeochemical redox processes also play an important role in the degradation of organic pollutants in the environment. The redox cycling of Fe and Mn mineral phases has been shown to be of particular importance for understanding contaminant fate and transport in a wide variety of environmental systems. For example, redox cycling of contaminants and host soil mineral phases can facilitate transport in surface water and groundwater posing a threat to water quality, as has been shown for a variety of different compounds (e.g., As, U, Cr, P). Because of their ubiquity and redox reactivity, reactions involving Feand Mn-minerals can be the key to understanding contaminant mobility in soil/sediment systems. Research into biogeochemical redox processes is more than a purely intellectual pursuit; a profound understanding of redox processes can be utilized for developing novel remediation strategies. Of notable success is zerovalent Fe permeable reactive barriers as a cost-effective method for treating groundwater for a variety of (chloro)organic compounds, nitrate, and reductive precipitation of certain trace metals and radionuclides (e.g., Cr and U). There has also been considerable interest in field-scale in situ biostimulation for sequestration of trace metals and radionuclides from groundwater. Native metal-reducing microbial communities are stimulated by amending groundwater with an electron donor such as ethanol or acetate, resulting in reductive precipitation of elements which are immobile when reduced, such as U and Cr. In addition, understanding biogeochemical redox conditions that lead to As mobilization in groundwater, or that can be used for As removal from drinking water, is helping to mitigate the health crisis in southeast Asia, where millions of people in Bangladesh, India, Cambodia, and Vietnam are exposed to high concentrations of naturally occurring As. The complexity inherent in environmental systems has and will continue to pose major challenges, but recent developments in analytical techniques have yielded new opportunities for a greater depth of understanding of biogeochemical redox processes. The role of spatial heterogeneity, the kinetics of coupled redox processes, the dynamics of microbial communities, electron transfer mechanisms, and redox-induced mineral transformations are only some of the future research needs. The availability of synchrotron-based spectroscopy and mapping techniques has revolutionized our ability to observe redox transformations at the micrometer to molecular scale. Various novel in situ electrode and gel probe techniques allow for direct, field-scale observation of redox processes with minimal disturbance of the system of interest. In addition, advances in instrumentation and sample preservation have increased our ability to detect redox-sensitive or ultratrace quantities of important species in the environment. A combination of field studies, novel experimental approaches, analytical techniques, and advanced computational tools will lead to exciting new findings over the coming years. The enormous progress made in many aspects of redox biogeochemistry in recent years has motivated us to pro-

Biogeochemical Controls of Uranium Bioavailability from the Dissolved Phase in Natural Freshwaters.

To gain insights into the risks associated with uranium (U) mining and processing, we investigated the biogeochemical controls of U bioavailability in the model freshwater species Lymnaea stagnalis (Gastropoda). Bioavailability of dissolved U(VI) was characterized in controlled laboratory experiments over a range of water hardness, pH, and in the presence of complexing ligands in the form of dissolved natural organic matter (DOM). Results show that dissolved U is bioavailable under all the geochemical conditions tested. Uranium uptake rates follow first order kinetics over a range encompassing most environmental concentrations. Uranium uptake rates in L. stagnalis ultimately demonstrate saturation uptake kinetics when exposure concentrations exceed 100 nM, suggesting uptake via a finite number of carriers or ion channels. The lack of a relationship between U uptake rate constants and Ca uptake rates suggest that U does not exclusively use Ca membrane transporters. In general, U bioavailability decreases with increasing pH, increasing Ca and Mg concentrations, and when DOM is present. Competing ions did not affect U uptake rates. Speciation modeling that includes formation constants for U ternary complexes reveals that the aqueous concentration of dicarbonato U species (UO2(CO3)2(-2)) best predicts U bioavailability to L. stagnalis, challenging the free-ion activity model postulate.

Structured Populations of Sulfolobus acidocaldarius with Susceptibility to Mobile Genetic Elements

Abstract The impact of a structured environment on genome evolution can be determined through comparative population genomics of species that live in the same habitat. Recent work comparing three genome sequences of Sulfolobus acidocaldarius suggested that highly structured, extreme, hot spring environments do not limit dispersal of this thermoacidophile, in contrast to other co-occurring Sulfolobus species. Instead, a high level of conservation among these three S. acidocaldarius genomes was hypothesized to result from rapid, global-scale dispersal promoted by low susceptibility to viruses that sets S. acidocaldarius apart from its sister Sulfolobus species. To test this hypothesis, we conducted a comparative analysis of 47 genomes of S. acidocaldarius from spatial and temporal sampling of two hot springs in Yellowstone National Park. While we confirm the low diversity in the core genome, we observe differentiation among S. acidocaldarius populations, likely resulting from low migration among hot spring “islands” in Yellowstone National Park. Patterns of genomic variation indicate that differing geological contexts result in the elimination or preservation of diversity among differentiated populations. We observe multiple deletions associated with a large genomic island rich in glycosyltransferases, differential integrations of the Sulfolobus turreted icosahedral virus, as well as two different plasmid elements. These data demonstrate that neither rapid dispersal nor lack of mobile genetic elements result in low diversity in the S. acidocaldarius genomes. We suggest instead that significant differences in the recent evolutionary history, or the intrinsic evolutionary rates, of sister Sulfolobus species result in the relatively low diversity of the S. acidocaldarius genome.