Table of Contents
Advances in Ecology
Volume 2014, Article ID 786929, 14 pages
http://dx.doi.org/10.1155/2014/786929
Review Article

Phosphate-Mediated Remediation of Metals and Radionuclides

Department of Biological Sciences, University of Alabama, 300 Hackberry Lane, Tuscaloosa, AL 35487, USA

Received 24 March 2014; Accepted 10 July 2014; Published 11 September 2014

Academic Editor: Alistair Bishop

Copyright © 2014 Robert J. Martinez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Worldwide industrialization activities create vast amounts of organic and inorganic waste streams that frequently result in significant soil and groundwater contamination. Metals and radionuclides are of particular concern due to their mobility and long-term persistence in aquatic and terrestrial environments. As the global population increases, the demand for safe, contaminant-free soil and groundwater will increase as will the need for effective and inexpensive remediation strategies. Remediation strategies that include physical and chemical methods (i.e., abiotic) or biological activities have been shown to impede the migration of radionuclide and metal contaminants within soil and groundwater. However, abiotic remediation methods are often too costly owing to the quantities and volumes of soils and/or groundwater requiring treatment. The in situ sequestration of metals and radionuclides mediated by biological activities associated with microbial phosphorus metabolism is a promising and less costly addition to our existing remediation methods. This review highlights the current strategies for abiotic and microbial phosphate-mediated techniques for uranium and metal remediation.

1. Introduction

The global population is predicted to reach 10 billion by the year 2100 [1]. To support the demand for increased food production and access to fresh water, human societies will be forced to employ less desirable (i.e., lower quality) soil and groundwater resources for crop production and drinking water [13]. Human activities associated with 20th century industrial-scale production of electrical components, fabrics, fertilizers, inks and dyes, mining, metal production, paints, paper products, pesticides, pharmaceuticals, rubber, and plastics contribute to the degradation of surface and subsurface sediments and water quality as evidenced by the production of more than 1 million metric tons of metal waste per year [4, 5]. Governmental activities have also contributed to the contamination of soils and groundwater throughout the United States, where the legacy of nuclear weapons research and development has resulted in the contamination of estimated 75 million cubic meters of sediment and more than 1.8 billion cubic meters of groundwater [6]. The devastating 2011 earthquake of the coast of Japan and the subsequent tsunami that destroyed three nuclear reactors at the Fukushima Daiichi Nuclear Power Plant complex highlight a more recent challenge to remediation and disposal of large quantities of nuclear fuel materials including radionuclides. The scope of the remediation challenge is considerable, as deleterious effects to human health, surrounding environment, and food supply are well known due to metal and radionuclide exposure and ingestion [710]. Moreover, the presence of these contaminants negatively impacts ecosystem sustainability and contribute to the loss of biodiversity [11].

Lead (Pb), cadmium (Cd), and zinc (Zn) represent a subset of the most frequently reported metal contaminants in sediments and groundwater. These metals, many of which cooccur at the same site, are listed on the US EPA National Priorities List and are detected at many US EPA Superfund sites [12]. Uranium (U) waste, resulting from U.S. nuclear weapons production, is found in soils and groundwater at the Department of Energy (DOE) facilities [13] and in coal and phosphate mining/processing waste sites [1419]. The fate and transport of metals and radionuclides in the environment are controlled by geochemical factors, including pH, adsorption, reduction/oxidation, and precipitation reactions. In natural environments, pH is one of the primary controlling variables for metal and radionuclide speciation [20]. Below pH ~5, most metals and radionuclides tend to exist primarily as free divalent cations and as solid oxyhydroxides, carbonates, and oxides above pH 7 (Figures 1(a) and 1(b)). In the presence of phosphate, precipitation reactions control metal speciation through the formation of highly insoluble metal- and radionuclide-phosphate minerals that are stable over a wide pH range (Figures 2(a) and 2(b)). Though less studied to date than other methods, remediation approaches that promote phosphate immobilization of metals and radionuclides represent viable strategies for long-term in situ sequestration.

fig1
Figure 1: Influence of changing pH on chemical speciation of (a) U(VI) and (b) metal mixture composed of Cd(II), Pb(II), and Zn(II). Calculated using MINEQL + v. 4.5 and the Nuclear Energy Agency’s updated thermodynamic database for uranium [106, 107] as a function of pH in synthetic groundwater (SGW). The open system model at 22°C calculated aqueous (dotted lines) and solid phases (solid lines) at equilibrium using the concentrations of ions present in SGW, μM, μM, μM, μM, and  atm. Chemical speciation calculations utilized SGW that consists of 2 μM FeSO4, 5 μM MnCl2, 8 μM Na2MoO4, 0.8 mM MgSO4, 7.5 mM NaNO3, 0.4 mM KCl, 7.5 mM KNO3, and 0.2 mM Ca (NO3)2 [57].
fig2
Figure 2: Influence of soluble phosphate and changing pH on chemical speciation of (a) U(VI) and (b) metal mixture composed of Cd(II), Pb(II), and Zn(II), Calculated using MINEQL + v. 4.5 and the Nuclear Energy Agency’s updated thermodynamic database for uranium [106, 107] as a function of pH in synthetic groundwater (SGW). The open system model at 22°C calculated aqueous (dotted lines) and solid phases (solid lines) at equilibrium using the concentrations of ions present in SGW, μM, μM, μM, μM, μM, and  atm. Chemical speciation calculations utilized SGW that consists of 2 μM FeSO4, 5 μM MnCl2, 8 μM Na2MoO4, 0.8 mM MgSO4, 7.5 mM NaNO3, 0.4 mM KCl, 7.5 mM KNO3, and 0.2 mM Ca (NO3)2 [57].

Strategies for the remediation of metal and radionuclide-contaminated soils and groundwater include physical and chemical (i.e., abiotic) and biologically mediated methods. Chemical and physical methods, including excavation and soil capping [21, 22], pump and treat technologies [23, 24], mineral adsorption [2527], mineral precipitation [28, 29], complexation [3032], adsorption to permeable zero-valent iron and hydroxyapatite reactive barriers [3335], cement solidification [36, 37], and vitrification [38, 39], have all demonstrated efficacy in mitigating contaminant transport in situ. Remediation methods that depend upon chemical transformations for in situ sequestration of contaminants must first consider local geochemical parameters that include local geology, concentrations of soluble anions and cations, pH, and redox state. The influence of pH on a contaminated groundwater system (Figures 1(a) and 1(b)) highlights the importance of such considerations in order to predict contaminants speciation and bioavailability [4044].

In addition to the chemically mediated methods for contaminant immobilization, bioremediation has demonstrated great promise as an additional strategy to promote in situ sequestration of contaminants [11, 4548] by harnessing the metabolisms of plants and microorganisms to detoxify and/or affect the in situ mobility of a given contaminant. The use of prokaryotic and eukaryotic microorganisms has proven effective for metal and radionuclide remediation through the processes of biosorption, bioaccumulation, bioreduction, and biomineralization [4961]. Recently, it has been shown that microorganisms, which can hydrolyze organophosphate compounds with a concomitant increase in the liberation of extracellular orthophosphate to the surrounding environment, represent a unique approach to promote subsurface in situ phosphate biomineralization of metals and radionuclides. The stability of phosphate minerals over a broad pH range (Figures 2(a) and 2(b)) provides an ideal insoluble phase for long-term contaminant sequestration within subsurface environments that experience changing local geochemistry (e.g., Eh, pH, oxidants).

The application of various phosphate compounds (e.g., orthophosphate solutions, soluble polyphosphates, and organophosphates) to immobilize contaminants (e.g., Cd, Pb, U, and Zn) in laboratory as well as field experiments detected contaminant sequestration via a combination of microbial-mediated mechanisms and abiotic reactions. The focus of this review will be on the chemical (abiotic) and microbial mechanisms promoting phosphate-mediated immobilization of uranium and cooccurring metals (Figure 3) within subsurface environments as well as highlighting the unique challenges that dynamic geochemical conditions have on long-term in situ sequestration strategies.

786929.fig.003
Figure 3: Flow-chart summary of chemical- and microbial-mediated reactions with phosphate that promote immobilization of metal and radionuclide contaminants within subsurface environments.

2. Chemical Approaches to Phosphate Immobilization of Metals and Radionuclides

The chemistry of phosphate is such that it facilitates reactions with over 30 elements and has resulted in the identification of 300 unique phosphate minerals [62]. On Earth, 95% of all phosphorus (P) is present within apatite minerals [Ca5(PO4)3(F,OH,Cl)] [63, 64] and the biogeochemical interactions of this mineral not only play a role in global P cycling but also influence the mobility of soluble metals [65]. The use of orthophosphate solutions has been shown to immobilize contaminants (e.g., Cd, Pb, U, and Zn) via mineral precipitation over a broad pH range (Figures 2(a) and 2(b)) [6669]. Additionally, phosphate minerals promote cocontaminant sequestration via mineral substitution reactions, coprecipitation reactions, adsorption, and ion-exchange reactions and provide a source of orthophosphate for dissolution-precipitation reactions [34, 7076]. Various soluble and insoluble P compounds (e.g., orthophosphate solutions, soluble polyphosphate, phosphatidic clays, apatite reactive barriers, and vivianite) have demonstrated success in metal and radionuclide sequestration [34, 68, 7785].

2.1. Soluble Phosphate Amendments

Soluble P, in the forms of phosphoric acid, phytic acid, and tripolyphosphate, has been examined for the sequestration of Cd, Cu, Pb, U, and Zn in contaminated environments [78, 82, 84, 8688]. Phosphoric acid and inorganic phosphate salts are examples of simple forms of reactive orthophosphate effective in forming stable minerals in surface soils (depth < 12.5 cm) contaminated with Cd, Cu, Pb, and Zn [8789]. The use of orthophosphate solutions within surface soils and deep subsurface environments requires strategies that prevent (1) rapid precipitation of contaminants and other sediment components (e.g., Al, Ca, Fe, Mg, and Mn) that affects hydraulic conductivity, (2) leaching of metals (e.g., As, Se, and W), and (3) ecosystem eutrophication caused by excess P runoff [82, 8991].

Compounds such as phytic acid (i.e., the acid form of inositol-6-phosphate) and polyphosphate have been examined for their ability to (1) act as sites for ion exchange, (2) facilitate the slow delivery of orthophosphate, and (3) act as chelating agents that minimize the bioavailability of cations within contaminated environments [9295]. The use of these compounds will ideally minimize undesirable phosphate-sediment interactions at the site of delivery, allow for greater mobility beyond the point of injection within subsurface sediments, and promote greater sequestration of metals and/or radionuclides when compared to injections of orthophosphate-rich solutions.

Laboratory studies examining the immobilization of various cations (i.e., Ba, Co, Mn, Ni, Pb, U, and Zn) within contaminated sediments have shown phytic acid to be effective in reducing soluble contaminant concentrations. Specifically, concentrations of U(VI) were reduced from 2,242 g kg−1 to 76 g kg−1 and of Ni from 58 mg kg−1 to 9.6 mg kg−1 in sediment batch incubations treated with calcium phytate (i.e., the salt of phytic acid) [92, 93]. However, the solubility of these metal-phytate complexes is highly dependent upon ionic strength, pH, ligand conformation, and metal-to-ligand ratio [96], which limits the efficacy of phytic acid for metal and radionuclide immobilization in dynamic geochemical conditions. More recent studies of phytic acid, sodium monophosphate, and sodium tripolyphosphate (TPP) interactions with U(VI) conducted in column experiments investigated sediments with basic porewater pH and geochemical conditions representative of metal- and radionuclide-contaminated environments in the western U.S. [82, 84]. In column studies, without soluble U, cation interactions with phytic acid and sodium monophosphate resulted in a 30% decrease in hydraulic conductivity [82]. Conversely, TPP amendments did not affect hydraulic conductivity and allowed for a slow release of orthophosphate within the sediment column [82]. Within columns containing over 100 mg L−1 soluble U, TPP amendments were capable of promoting rapid precipitation of U, thereby decreasing U concentrations below U.S. EPA drinking water standards (30 μg L−1) [84]. The use of TPP, rather than phytic acid or sodium monophosphate, demonstrates great promise within neutral-to-alkaline sediments as an agent for metal and radionuclide sequestration.

2.2. Solid Reactive Phosphate Amendments

An alternative to introducing soluble orthophosphate into contaminated sediment and groundwater is the application of apatite [Ca5(PO4)3(F,OH,Cl)] minerals (e.g., bone apatite, synthetic apatite minerals, and rock phosphate) as subsurface reactive barriers [97102]. Numerous studies have demonstrated that in situ soluble metal and radionuclide concentrations can be greatly reduced by surface interactions, dissolution-precipitation reactions, and ion-exchange with apatite minerals [34, 70, 73, 103, 104]. Apatite minerals have been effective in decreasing soluble concentrations (i.e., a 1,000-fold reduction) of contaminants that include Cd, Co, Cu, Hg, Mn, Ni, Pb, Sb, Th, and U [73, 79, 105]. Apatite reactive barriers have been effective in decreasing soluble metal and radionuclide concentrations in situ; however, the reversibility of cation adsorption and possible changes to hydraulic conductivity must be considered with this approach [34, 80, 81, 100]. Thus, the use of apatite requires continuous monitoring of the barrier effluent under dynamic geochemical conditions (i.e., changing contaminant concentration and pH) to maintain optimal contaminant sequestration and to calculate barrier lifetime [80, 100].

Recent studies have demonstrated promising results in the use of phosphate mineral nanoparticles for the remediation of Cu, Cd, and Pb contaminants [83, 108, 109]. The use of hydroxyapatite and vivianite [Fe3(PO4)2] nanoparticles in the size range of 3–10 nm provides properties of both liquid and solid phosphate amendments by facilitating liquid injection of particles that have a high surface area. Additionally, the use of nanoparticles offers an approach that maximizes contaminant immobilization by minimizing (1) orthophosphate loss to runoff, (2) precipitation reactions at the injection site, and (3) leaching of oxyanions. The unique application of phosphate mineral phases in the nanoparticle size range not only offers an effective delivery system to promote contaminant adsorption, precipitation, and/or ion-exchange reactions, but also provides a source of P to deep subsurface microbial communities capable of catalyzing reactions that further contribute to contaminant sequestration. Due to the lack of studies that examine nanoparticle fate and transport as well as the difficulties in monitoring this class of material in the environment, the potential hazards posed to prokaryotes, plants, and animals must be evaluated prior to their implementation in any remediation strategies [110112].

3. Biological Approaches to Phosphate-Mediated Immobilization of Metals and Radionuclides

Phosphorus in the form of inorganic phosphate (Pi) is essential for cellular energy conservation and proper structure/function of cellular macromolecules (i.e., nucleic acids, proteins, sugars, and lipids) in all living organisms [113]. Due to the essential requirement for P, the scarcity of this nutrient within terrestrial environments (i.e., average of 1 μM [114]) requires plants, fungi, and bacteria to employ P-scavenging strategies. Bacterial acquisition of P can occur through secretion of organic acids that solubilize phosphate minerals via expression of organophosphate hydrolases [115124]. Conversely, microbial stress (i.e., low nutrients, low pH, and oxidizing agents) results in storage of P as intracellular polyphosphate [125127]. The following sections will specifically examine microbial polyphosphate metabolism and organophosphate hydrolase activity as they relate to metal and radionuclide immobilization.

3.1. Polyphosphate-Mediated Bioaccumulation

The biologically mediated polymerization of orthophosphate molecules as intracellular polyphosphate granules is among the most ancestral metabolic functions present in all domains of life [125]. In bacteria, this polymer has been shown to function as an energy source, P reserve, metal chelator, and a regulator of stress and development [125, 127]. Polyphosphate metabolism in E. coli and other bacterial species is driven by the genes polyphosphate kinase (ppk) and exopolyphosphatase (ppx) that catalyze intracellular inorganic phosphate polymerization and hydrolysis of polyphosphate granules, respectively [125]. Phenotypic analyses of ppk knock-out mutations have expanded the known functions of polyphosphates that contribute to virulence, motility, biofilm formation, and sensitivity to stressors (e.g., oxidative, heat, osmotic, pH, and nutrient) [125127]. Within metal and radionuclide contaminated environments, low nutrient availability, high concentrations of oxidizing agents, and extremes in pH typify chemical stressors that pose challenges to microbial metabolism. In response to the local geochemistry of contaminated environments, production of intracellular polyphosphate provides microorganisms with a means to sequester toxic ions within the cell cytosol as well as the regulation of gene(s) expressed in response to cellular stress (e.g., DNA repair, RNA polymerase sigma factor, and pH extremes) [55, 127131].

The reactivity of cytosolic polyphosphates has been shown to facilitate intracellular sequestration of Cd, Cu, Hg, Pb, U, and Zn in genetically engineered bacterial strains as well as naturally occurring archaeal and bacterial strains [52, 55, 132136]. Electron microscopy analyses of cells exposed to these elements demonstrated intracellular localization with phosphate-rich granules, suggesting that contaminant sequestration may be achieved by polyphosphates and may protect sensitive cytosolic molecules from oxidative damage. In addition to polyphosphate chelation of metals and radionuclides, an engineered Pseudomonas aeruginosa strain overexpressing the ppk gene was shown to enhance intracellular phosphate concentrations when compared to the wild-type strain [133]. Upon nutrient starvation, polyphosphate depolymerization and efflux of phosphate into the media containing U(VI) promoted the removal of 80% of the soluble U(VI) as a uranyl phosphate precipitate. Thus, polyphosphate metabolism that promotes intracellular or extracellular sequestration of metals and radionuclides represents a remediation approach that harnesses the physiologies of extant microorganisms within contaminated environments.

3.2. Phosphatase-Mediated Biomineralization

Redox-independent biomineralization of metals and radionuclides, although not as extensively studied as reductive precipitation to date, could provide a complementary approach to the existing remediation strategies. Biogenically derived phosphate minerals result from the activities of microbial phosphatases, enzymes that are essential for microbial acquisition of C and P, regulation of cellular metabolism, and signal transduction [137139]. Phosphatase enzymes are classified by pH optima (acid or alkaline), molecular weight, and those that hydrolyze only phosphorylated serine or threonine residues [140]. Acid and alkaline phosphatases (either cytoplasmic or periplasmic) are fundamentally required for microbial nutrient acquisition [116, 119, 141143].

Early work examining bacteria capable of phosphate-mediated biomineralization of metals and radionuclides focused on the acid phosphatase activity of Serratia sp. NCIMB 40259 (formerly Citrobacter species) [50, 144, 145]. Several studies that characterized Class A NSAP of Serratia sp. NCIMB 40259 reported that microorganisms with similar phosphatase activities could be exploited to promote mineralization of metals [50, 144146]. Additionally, biofilms of Serratia sp. NCIMB 40259 that promoted the precipitation of H2(UO2)2(PO4)2 (chernikovite) further removed 85% and 97% of cooccurring 60Co and 137Cs, respectively, via substitution of H+ within chernikovite [147].

Prior to investigations into a possible bioremediation role for nonspecific acid phosphatases (NSAP), this class of enzymes had been examined for their role in microbial physiology and contributions to virulence [116, 148]. Although the exact physiological roles for these enzymes have yet to be discerned, the biochemical properties of NSAPs have been well studied. NSAPs are divided into three unique classes (Classes A, B, and C) based on catalytic domain motifs, comprised of low molecular weight monomeric subunits ranging from 25 to 30 kDa, and have a pH optima ranging from 5.0 to 6.5 and catalytic activities for a broad range of phosphomonoester substrates [116]. NSAPs can be localized to the outer membrane, periplasmic space and/or are secreted into the extracellular environment. As the physiological properties of bacterial NSAPs facilitate their activities at low pH conditions typical of many mixed waste sites, their contributions to in situ metal detoxification and metal immobilization activities may be greatly underappreciated.

Within mixed waste environments, the in situ activities of microbial phosphatases likely contribute to localized cation precipitation in addition to nutrient acquisition. Studies examining phosphatase activities (e.g., alkaline or acid) of genetically engineered and naturally occurring strains of Gram-positive and Gram-negative bacteria were shown to promote U immobilization (>90% precipitation of soluble U) via precipitation and coprecipitation reactions [50, 57, 60, 74, 149153]. Interestingly, soil bacterial isolates demonstrated constitutive phosphatase activities that liberated comparable, if not greater concentrations, of reactive phosphate when compared to the phosphatase activities of genetically modified strains [57, 149]. The occurrence of naturally occurring bacteria with constitutive phosphate-liberating NSAP phenotypes isolated from radionuclide and metal contaminated subsurface soils supports the role of acid phosphatases in promoting microbial adaptation to in situ metal stresses.

To further highlight such adaptation, recent investigations of terrestrial and marine bacterial isolates belonging to the genera Aeromonas, Bacillus, Myxococcus, Pantoea, Pseudomonas, Rahnella, and Vibrio demonstrated that Cr, Pb, and U were removed from solution as phosphate minerals under both oxic and anoxic growth conditions [57, 60, 74, 152, 154158]. Our recent work further examined lead and uranium precipitates produced by Rahnella sp. Y9602, using X-ray diffraction (XRD), variable pressure scanning electron microscopy/energy dispersive X-ray spectroscopy (VP-SEM/EDX), and extended X-ray absorption fine structure (EXAFS). Hydrated lead precipitates that accumulated on the cell surface of Rahnella sp. Y9602 were identified as lead hydroxyapatite, Pb10(PO4)6(OH)2 by XRD analysis (data unpublished). VP-SEM/EDX elemental mapping demonstrated U and P localization in precipitates generated by Rahnella sp. Y9602 grown in minimal media containing soluble U(VI). Subsequent synchrotron-based XRD and EXAFS analyses of these uranium phosphate precipitates identified the mineral as chernikovite [H2(UO2)2(PO4)2] [60].

4. Challenges for In Situ Immobilization of Metals and Radionuclides

The goal of metal and/or radionuclide remediation strategies that focus on in situ sequestration is to generate an insoluble precipitate that will be immobilized, sequestered, and stable within a given environment for effective long-term stewardship. The difficulty in maintaining precipitates in the solid phase arises from the dynamic nature of biogeochemical processes in the environment.

Approaches that employ reductive precipitation of metals and radionuclides through the use of zero-valent iron reactive barriers, mineral phase interactions, and microbial reduction activities face challenges for long-term sequestration that arise from oxidant (e.g., oxygen, nitrate, manganese, iron oxides, or humic substances) interactions that remobilize precipitated reduced contaminants to their oxidized valence states, thereby increasing their solubility [19, 45, 159168]. Limitations to microbial reduction of metals and radionuclide also arise from low pH environments that must be neutralized to support growth of sulfate- and metal-reducing communities [163, 169, 170]. Additionally, microbial reduction in mixed waste environments must be carefully considered so as to minimize contaminant migration of elements such as As and Pu that demonstrate greater mobility in their reduced valence states [171, 172].

In contrast, the geochemical stability of insoluble metal- and radionuclide-phosphates allows for in situ sequestration within environments that undergo dynamic changes in redox conditions and pH. Such changes, in local geochemistry, however, do not support stable sequestration of metals and radionuclides in their reduced forms. Within uranium contaminated environments, phosphate mineralization of soluble U(VI) produces a wide array of uranyl phosphate minerals [173]. The formation of these minerals has been implicated in the control of U mobility in U.S. DOE contaminated sediments [174, 175], although the microbial contribution to in situ uranyl phosphate formation in these DOE sites has yet to be determined. With recent studies identifying autunite- and hydroxyapatite-precipitating capabilities of Aeromonas, Bacillus, Pantoea, Pseudomonas, and Rahnella spp. in both oxic and anoxic growth conditions, the synergistic properties of these minerals (i.e., ion-exchange reactions that sequester cooccurring metals) highlight an important role in not only stabilizing U contamination but also cooccurring metals [57, 60, 74, 157]. Furthermore, contaminated sites that are characterized by acidic to circumneutral porewater pH represent environments that can support stable mineral formation (Figures 2(a) and 2(b)), provided that carbonates are not present in significant concentrations (i.e., < 10−3.5 atm) [176, 177]. Interestingly, investigations of microbial reduction of Cr, Np, Pu, and U have been shown to support subsequent phosphate precipitation reactions via thermodynamic modeling, chromatographic separation of actinides based on valence state, and X-ray analytical methods [154, 155, 172, 178, 179]. Unlike U, that is capable of forming phosphate minerals in both hexavalent and tetravalent states [50, 179], the reduction of Cr, Np, and Pu is initially required for these contaminants to participate in phosphate precipitation reactions [154, 155, 172, 178]. To date, only pure culture or coculture studies have identified such coupled microbial interactions that offer an additional approach to control contaminant toxicity and mobility that are perpetuated by valence state cycling. Due to the limited number of studies, future work is required to further understand protocooperative interactions between extant subsurface metal reducing and phosphate solubilizing microbial communities that promote contaminant sequestration. Additionally, further examination of reduced valence state contaminants precipitated as phosphate minerals are required to understand the influence of changing geochemical parameters (e.g., Eh, pH, and oxidants) that can affect solubility of the in situ immobilized contaminants.

Overall, these studies highlight the need to consider contaminant physicochemical properties, redox state of the environment, pH, presence of complexing ligands, and the metabolic properties of the extant microbial community when developing an in situ sequestration strategy.

5. Summary, Challenges, and Future Directions

Prior to anthropogenic releases of metals and radionuclides into the environment, these elements had been (and continue to be) discharged into the environment through volcanic activity, hydrothermal vent sources, and the dissolution of metal-bearing minerals [180]. Prokaryotic and eukaryotic organisms play key roles in geochemical cycling through metabolic processes that scavenge, mobilize, and precipitate these elements in terrestrial, aquatic, and atmospheric environments [180182]. The evolution of prokaryotic and eukaryotic organisms that influence the solubility of metal- and radionuclide-bearing minerals while tolerating changing concentrations of these elements has given rise to microbial metabolic diversity beneficial to passive and active environmental remediation efforts.

Passive remediation approaches such as monitored natural attenuation (MNA) and in situ sequestration of metals and radionuclides offer economical alternatives that minimize human exposure to contaminants. Regardless of the type of implemented remediation approach, successful in situ sequestration of metals and radionuclides requires the contaminant(s) remain immobilized as an insoluble species. Implementation of MNA of metals and radionuclides relies on natural physical, chemical, and biological processes to remediate a contaminated environment through the effects of dispersion, dilution, sorption, volatilization, radioactive decay, stabilization, and transformation [183]. Prior to adopting MNA as a sole strategy for metal and radionuclide remediation, the processes by which the contaminant(s) are immobilized must be shown to be irreversible [183]. Unfortunately, this approach relies on limited contaminant plume mobility as well as stable geochemical and hydrological conditions [183187]. Therefore, contaminated subsurface environments with changing hydrobiogeochemical conditions (typical for most sites) will likely influence speciation chemistry and thus require an alternative strategy.

Active remediation strategies that promote metal- and/or radionuclide-phosphate formation can take advantage of in situ hydrobiogeochemical parameters (Figure 4) that support contaminant sequestration through the formation of (1) low solubility minerals that are unaffected by changes in redox, (2) mineral stability across a wide pH range, and (3) reactive mineral surfaces that can support sequestration of other cooccurring metals through adsorption, substitution, and precipitation reactions [60, 83, 109, 147, 154, 188]. Innovative bioremediation approaches that neutralize low pH groundwater and maintain sufficient phosphate concentrations to complex soluble contaminants can enhance strategies that rely solely on abiotic approaches. By employing a phosphate-mediated pH buffering system, soluble U(VI) can be sequestered as insoluble uranyl hydroxide and uranyl phosphate species [157, 189]. Unlike uraninite (UO2) mediated sequestration, uranyl phosphate species are not prone to dissolution in oxidizing environments. Thermodynamic modeling and recent anaerobic biomineralization assays utilizing Rahnella sp. Y9602 and U contaminated sediments have shown that uranium phosphate formation can be promoted by microbial hydrolysis of organophosphate substrates under reducing conditions [60, 190].

786929.fig.004
Figure 4: Subsurface hydrobiogeochemical conceptual model. Important chemical and microbial mediated processes that control metal speciation and contaminant transport within subsurface sediments include (a) Fe-hydroxide surface (clays) adsorption; (b) sediment organic matter adsorption; (c) microbial detoxification mechanisms contributing to microbial survival, adaptation, and contaminant immobilization. Microbial metabolic processes that increase local concentrations of anions (; e.g., , , and ) promote inorganic contaminant () mineralization [].

To date, the majority of metal and radionuclide immobilization studies have focused on bacterial physiology and ecology without considering concomitant archaeal and fungal community responses and/or contributions made by members of these two domains of life. Additional studies that include detailed analyses of archaeal, bacterial, and fungal activities that may be contributing to the mineralization of metals and radionuclides through phosphate-driven mechanisms are needed if we are to have a complete understanding of microbial community responses as they relate to phosphate-mediated bioremediation strategies [122, 135, 191193]. Interdisciplinary studies that combine analyses of microbial communities and geochemical dynamics are essential to provide a greater understanding of in situ processes that affect contaminant sequestration.

New and emerging methods, such as metagenomics and metaproteomics, which allow for a greater understanding of microbe-metal interactions, many of which were pioneered as a result of academic and U.S. Department of Energy National Laboratory collaborations, have yielded significant insights into subsurface microbial community dynamics and physiological responses within contaminated environments [194206]. Additionally, synchrotron X-ray techniques (e.g., XRD, XANES, and EXAFS) have become tools for biogeochemical studies that enhance our understanding of in situ contaminant sequestration. Recent studies that incorporate X-ray techniques have elucidated U interactions with sediment surfaces and biomass as well as facilitated mineral identification [60, 153, 179, 207209]. Combining results from such interdisciplinary studies need to be placed in the context of the whole “in terra” system for long-term field-scale applications [210]. Ultimately, the combined efforts of interdisciplinary research focused on microbial P cycling will support development of predictive models necessary to understand the challenges of long-term contaminant sequestration within geochemically dynamic environments.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgment

The authors wish to thank the U.S. Department of Energy, Office of Science (BER), for providing support through U.S. Department of Energy, Grant no. DE-FG02-04ER63906.

References

  1. NRC, Our Common Journey: A Transition Toward Sustainability, National Academies Press, Washington, DC, USA, 1999.
  2. D. Tilman, K. G. Cassman, P. A. Matson, R. Naylor, and S. Polasky, “Agricultural sustainability and intensive production practices,” Nature, vol. 418, no. 6898, pp. 671–677, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Bouwer, “Integrated water management for the 21st century: problems and solutions,” Journal of Irrigation and Drainage Engineering, vol. 128, no. 4, pp. 193–202, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. B. L. Morris, A. R. L. Lawrence, P. J. C. Chilton et al., Groundwater and its Susceptibility to Degradation: A Global Assessment of the Problem and Options for Management, United Nations Environment Programme, Nairobi, Kenya, 2003.
  5. USCB, Statistical Abstract of the United States 2009, United States Census Bureau, Washington, DC, USA, 2009.
  6. DOE, Linking Legacies, DOE/EM-319, United States Department of Energy, Washington, DC, USA, 1997.
  7. K. S. Kasprzak, “Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis,” Free Radical Biology and Medicine, vol. 32, no. 10, pp. 958–967, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Fukuda, “Chelating agents used for plutonium and uranium removal in radiation emergency medicine,” Current Medicinal Chemistry, vol. 12, no. 23, pp. 2765–2770, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Valko, H. Morris, and M. T. D. Cronin, “Metals, toxicity and oxidative stress,” Current Medicinal Chemistry, vol. 12, no. 10, pp. 1161–1208, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Galanis, A. Karapetsas, and R. Sandaltzopoulos, “Metal-induced carcinogenesis, oxidative stress and hypoxia signalling,” Mutation Research—Genetic Toxicology and Environmental Mutagenesis, vol. 674, no. 1-2, pp. 31–35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. J. C. Philp, S. M. Bamforth, I. Singleton, and R. M. Atlas, “Environmental pollution and restoration: a role for bioremediation,” in Bioremediation: Applied Microbial Solutions for Real-World Environmental Cleanup, R. M. Atlas and J. Philp, Eds., pp. 1–48, ASM Press, Washington, DC, USA, 2005. View at Google Scholar
  12. EPA, “Search Superfund Site Information,” 2013, http://cumulis.epa.gov/supercpad/cursites/srchsites.cfm.
  13. R. G. Riley, J. M. Zachara, and F. J. Wobber, Chemical Comtaminants on DOE Lands and Selection of Contamination Mixtures for Subsurface Science Research, DOE/ER-0547T, Energy UDo, Washington, DC, USA, 1992.
  14. C. Tamponnet, A. Martin-Garin, M.-A. Gonze et al., “An overview of BORIS: bioavailability of radionuclides in soils,” Journal of Environmental Radioactivity, vol. 99, no. 5, pp. 820–830, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Papastefanou, “Escaping radioactivity from coal-fired power plants (CPPs) due to coal burning and the associated hazards: a review,” Journal of Environmental Radioactivity, vol. 101, no. 3, pp. 191–200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. M. R. Palmer and J. M. Edmond, “Uranium in river water,” Geochimica et Cosmochimica Acta, vol. 57, no. 20, pp. 4947–4955, 1993. View at Publisher · View at Google Scholar · View at Scopus
  17. C. F. Jove Colon, P. V. Brady, M. D. Siegel, and E. R. Lindgren, “Historical case analysis of uranium plume attenuation,” Soil and Sediment Contamination, vol. 10, no. 1, pp. 71–115, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. T. M. Esat and Y. Yokoyama, “Variability in the uranium isotopic composition of the oceans over glacial-interglacial timescales,” Geochimica et Cosmochimica Acta, vol. 70, no. 16, pp. 4140–4150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Regenspurg, D. Schild, T. Schäfer, F. Huber, and M. E. Malmström, “Removal of uranium(VI) from the aqueous phase by iron(II) minerals in presence of bicarbonate,” Applied Geochemistry, vol. 24, no. 9, pp. 1617–1625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Langmuir, Aqueous Environmental Geochemistry, Prentice Hall, Upper Saddle River, NJ, USA, 1997.
  21. A. S. Knox, M. H. Paller, D. D. Reible, X. Ma, and I. G. Petrisor, “Sequestering agents for active caps—remediation of metals and organics,” Soil and Sediment Contamination, vol. 17, no. 5, pp. 516–532, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. C. N. Mulligan, R. N. Yong, and B. F. Gibbs, “An evaluation of technologies for the heavy metal remediation of dredged sediments,” Journal of Hazardous Materials, vol. 85, no. 1-2, pp. 145–163, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Chellam and D. A. Clifford, “Physical-chemical treatment of groundwater contaminated by leachate from surface disposal of uranium tailings,” Journal of Environmental Engineering, vol. 128, no. 10, pp. 942–952, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. W.-M. Wu, J. Carley, M. Fienen et al., “Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone,” Environmental Science & Technology, vol. 40, no. 12, pp. 3978–3985, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Cheng, M. O. Barnett, E. E. Roden, and J. Zhuang, “Effects of phosphate on uranium(VI) adsorption to goethite-coated sand,” Environmental Science and Technology, vol. 38, no. 22, pp. 6059–6065, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Z. Tang and R. J. Reeder, “Uranyl and arsenate cosorption on aluminum oxide surface,” Geochimica et Cosmochimica Acta, vol. 73, no. 10, pp. 2727–2743, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Vidal, M. J. Santos, T. Abrão, J. Rodríguez, and A. Rigol, “Modeling competitive metal sorption in a mineral soil,” Geoderma, vol. 149, no. 3-4, pp. 189–198, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Z. El Aamrani, L. Duro, J. de Pablo, and J. Bruno, “Experimental study and modeling of the sorption of uranium(VI) onto olivine-rock,” Applied Geochemistry, vol. 17, no. 4, pp. 399–408, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. W. Luo, S. D. Kelly, K. M. Kemner et al., “Sequestering uranium and technetium through co-precipitation with aluminum in a contaminated acidic environment,” Environmental Science and Technology, vol. 43, no. 19, pp. 7516–7522, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. G. J. Vazquez, C. J. Dodge, and A. J. Francis, “Interaction of uranium(VI) with phthalic acid,” Inorganic Chemistry, vol. 47, no. 22, pp. 10739–10743, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. G. J. Vazquez, C. J. Dodge, and A. J. Francis, “Interactions of uranium with polyphosphate,” Chemosphere, vol. 70, no. 2, pp. 263–269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Ozaki, T. Kimura, T. Ohnuki et al., “Association of europium(III), americium(III), and curium(III) with cellulose, chitin, and chitosan,” Environmental Toxicology and Chemistry, vol. 25, no. 8, pp. 2051–2058, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Noubactep, A. Schöner, and G. Meinrath, “Mechanism of uranium removal from the aqueous solution by elemental iron,” Journal of Hazardous Materials, vol. 132, no. 2-3, pp. 202–212, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. F. G. Simon, V. Biermann, and B. Peplinski, “Uranium removal from groundwater using hydroxyapatite,” Applied Geochemistry, vol. 23, no. 8, pp. 2137–2145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. R. D. Ludwig, D. J. A. Smyth, D. W. Blowes et al., “Treatment of arsenic, heavy metals, and acidity using a mixed ZVI-compost PRB,” Environmental Science and Technology, vol. 43, no. 6, pp. 1970–1976, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. Q. Y. Chen, M. Tyrer, C. D. Hills, X. M. Yang, and P. Carey, “Immobilisation of heavy metal in cement-based solidification/stabilisation: a review,” Waste Management, vol. 29, no. 1, pp. 390–403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Paria and P. K. Yuet, “Solidification-stabilization of organic and inorganic contaminants using portland cement: a literature review,” Environmental Reviews, vol. 14, no. 4, pp. 217–255, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. A. S. Barinov, G. A. Varlakova, S. V. Stefanovskii, and M. I. Ozhovan, “Change of structure and properties of vitrified radioactive wastes during long-time storage in an experimental repository,” Atomic Energy, vol. 105, no. 2, pp. 110–117, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. P. A. Bingham and R. J. Hand, “Vitrification of toxic wastes: a brief review,” Advances in Applied Ceramics, vol. 105, no. 1, pp. 21–31, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Boukhalfa, S. D. Reilly, and M. P. Neu, “Complexation of Pu(IV) with the natural siderophore desferrioxamine B and the redox properties of Pu(IV)(siderophore) complexes,” Inorganic Chemistry, vol. 46, no. 3, pp. 1018–1026, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. R. J. Reeder, M. A. A. Schoonen, and A. Lanzirotti, “Metal speciation and its role in bioaccessibility and bioavailability,” Reviews in Mineralogy and Geochemistry, vol. 64, pp. 59–113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. C. E. Halim, S. A. Short, J. A. Scott, R. Amal, and G. Low, “Modelling the leaching of Pb, Cd, As, and Cr from cementitious waste using PHREEQC,” Journal of Hazardous Materials, vol. 125, no. 1–3, pp. 45–61, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. J. R. Haas, T. J. Dichristina, and R. Wade Jr., “Thermodynamics of U(VI) sorption onto Shewanella putrefaciens,” Chemical Geology, vol. 180, no. 1–4, pp. 33–54, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. G. W. Bryan and W. J. Langston, “Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries,” Environmental Pollution, vol. 76, no. 2, pp. 89–131, 1992. View at Publisher · View at Google Scholar · View at Scopus
  45. W.-M. Wu, J. Carley, J. Luo et al., “In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen,” Environmental Science and Technology, vol. 41, no. 16, pp. 5716–5723, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Faybishenko, T. C. Hazen, P. E. Long et al., “In situ long-term reductive bioimmobilization of Cr(VI) in groundwater using hydrogen release compound,” Environmental Science & Technology, vol. 42, no. 22, pp. 8478–8485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Hong-Bo, C. Li-Ye, R. Cheng-Jiang, L. Hua, G. Dong-Gang, and L. Wei-Xiang, “Understanding molecular mechanisms for improving phytoremediation of heavy metal-contaminated soils,” Critical Reviews in Biotechnology, vol. 30, no. 1, pp. 23–30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Van Aken, P. A. Correa, and J. L. Schnoor, “Phytoremediation of polychlorinated biphenyls: new trends and promises,” Environmental Science and Technology, vol. 44, no. 8, pp. 2767–2776, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. D. R. Lovley, E. J. P. Phillips, Y. A. Gorby, and E. R. Landa, “Microbial reduction of uranium,” Nature, vol. 350, no. 6317, pp. 413–416, 1991. View at Publisher · View at Google Scholar · View at Scopus
  50. L. E. Macaskie, R. M. Empson, A. K. Cheetham, C. P. Grey, and A. J. Skarnulis, “Uranium bioaccumulation by a Citrobacter sp. as a result of enzymically mediated growth of polycrystalline HUO2PO4,” Science, vol. 257, no. 5071, pp. 782–784, 1992. View at Publisher · View at Google Scholar · View at Scopus
  51. A. J. Francis, C. J. Dodge, F. Lu, G. P. Halada, and C. R. Clayton, “XPS and XANES studies of uranium reduction by Clostridium sp.,” Environmental Science Technology, vol. 28, no. 4, pp. 636–639, 1994. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Pan-Hou, M. Kiyono, H. Omura, T. Omura, and G. Endo, “Polyphosphate produced in recombinant Escherichia coli confers mercury resistance,” FEMS Microbiology Letters, vol. 207, no. 2, pp. 159–164, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Barkay, S. M. Miller, and A. O. Summers, “Bacterial mercury resistance from atoms to ecosystems,” FEMS Microbiology Reviews, vol. 27, no. 2-3, pp. 355–384, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Malik, “Metal bioremediation through growing cells,” Environment International, vol. 30, no. 2, pp. 261–278, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Suzuki and J. F. Banfield, “Resistance to, and accumulation of, uranium by bacteria from a uranium-contaminated site,” Geomicrobiology Journal, vol. 21, no. 2, pp. 113–121, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Tsuruta, “Cell-associated adsorption of thorium or uranium from aqueous system using various microorganisms,” Water, Air, and Soil Pollution, vol. 159, no. 1, pp. 35–47, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. R. J. Martinez, M. J. Beazley, M. Taillefert, A. K. Arakaki, J. Skolnick, and P. A. Sobecky, “Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils,” Environmental Microbiology, vol. 9, no. 12, pp. 3122–3133, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. R. A. Sanford, Q. Wu, Y. Sung et al., “Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields,” Environmental Microbiology, vol. 9, no. 11, pp. 2885–2893, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. M. L. Merroun and S. Selenska-Pobell, “Bacterial interactions with uranium: an environmental perspective,” Journal of Contaminant Hydrology, vol. 102, no. 3-4, pp. 285–295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. M. J. Beazley, R. J. Martinez, P. A. Sobecky, S. M. Webb, and M. Taillefert, “Nonreductive biomineralization of uranium(VI) phosphate via microbial phosphatase activity in anaerobic conditions,” Geomicrobiology Journal, vol. 26, no. 7, pp. 431–441, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. G. M. Gadd, “Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment,” Journal of Chemical Technology and Biotechnology, vol. 84, no. 1, pp. 13–28, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. J. O. Nriagu, “Phosphate minerals,” in Phosphate Minerals: Their Properties and General Modes of Occurrence, J. O. Nriagu and P. B. Moore, Eds., pp. 1–137, Springer, Berlin, Germany, 1984. View at Google Scholar
  63. V. Smil, “Phosphorus in the environment: natural flows and human interferences,” Annual Review of Energy and the Environment, vol. 25, pp. 53–88, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. K. B. Föllmi, “The phosphorus cycle, phosphogenesis and marine phosphate-rich deposits,” Earth-Science Reviews, vol. 40, no. 1-2, pp. 55–124, 1996. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Rakovan, “Growth and surface properties of apatite,” Reviews in Mineralogy and Geochemistry, vol. 48, no. 1, pp. 51–86, 2002. View at Google Scholar · View at Scopus
  66. S. L. McGowen, N. T. Basta, and G. O. Brown, “Use of diammonium phosphate to reduce heavy metal solubility and transport in smelter-contaminated soil,” Journal of Environmental Quality, vol. 30, no. 2, pp. 493–500, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. X. D. Cao, L. Q. Ma, M. Chen, S. P. Singh, and W. G. Harris, “Impacts of phosphate amendments on lead biogeochemistry at a contaminated site,” Environmental Science and Technology, vol. 36, no. 24, pp. 5296–5304, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. T. T. Eighmy and J. D. Eusden Jr., “Phosphate stabilization of municipal solid waste combustion residues: geochemical principles,” Geological Society Special Publications, vol. 236, pp. 435–473, 2004. View at Publisher · View at Google Scholar · View at Scopus
  69. V. S. Mehta, F. Maillot, Z. Wang, J. G. Catalano, and D. E. Giammar, “Effect of co-solutes on the products and solubility of uranium(VI) precipitated with phosphate,” Chemical Geology, vol. 364, pp. 66–75, 2014. View at Publisher · View at Google Scholar
  70. J. S. Arey, J. C. Seaman, and P. M. Bertsch, “Immobilization of uranium in contaminated sediments by hydroxyapatite addition,” Environmental Science & Technology, vol. 33, no. 2, pp. 337–342, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. J. C. Seaman, J. S. Arey, and P. M. Bertsch, “Immobilization of nickel and other metals in contaminated sediments by hydroxyapatite addition,” Journal of Environmental Quality, vol. 30, no. 2, pp. 460–469, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Pan and M. E. Fleet, “Compositions of the apatite-group minerals: Substitution mechanisms and controlling factors,” Reviews in Mineralogy and Geochemistry, vol. 48, no. 1, pp. 13–49, 2002. View at Google Scholar · View at Scopus
  73. A. S. Knox, D. I. Kaplan, D. C. Adriano, T. G. Hinton, and M. D. Wilson, “Apatite and phillipsite as sequestering agents for metals and radionuclides,” Journal of Environmental Quality, vol. 32, no. 2, pp. 515–525, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. E. S. Shelobolina, H. Konishi, H. Xu, and E. E. Roden, “U(VI) sequestration in hydroxyapatite produced by microbial glycerol 3-phosphate metabolism,” Applied and Environmental Microbiology, vol. 75, no. 18, pp. 5773–5778, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. D. R. Brookshaw, R. A. D. Pattrick, J. R. Lloyd, and D. J. Vaughan, “Microbial effects on mineral-radionuclide interactions and radionuclide solid-phase capture processes,” Mineralogical Magazine, vol. 76, no. 3, pp. 777–806, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. I. Llorens, G. Untereiner, D. Jaillard, B. Gouget, V. Chapon, and M. Carriere, “Uranium interaction with two multi-resistant environmental bacteria: Cupriavidus metallidurans CH34 and Rhodopseudomonas palustris,” PLoS ONE, vol. 7, no. 12, Article ID e51783, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. S. P. Singh, L. Q. Ma, and W. G. Harris, “Heavy metal interactions with phosphatic clay: sorption and desorption behavior,” Journal of Environmental Quality, vol. 30, no. 6, pp. 1961–1968, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. J. Yang, D. E. Mosby, S. W. Casteel, and R. W. Blanchar, “Lead immobilization using phosphoric acid in a smelter-contaminated urban soil,” Environmental Science and Technology, vol. 35, no. 17, pp. 3553–3559, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. W. D. Bostick, Use of Apatite for Chemical Stabilization of Subsurface Contaminants, U.S. Department of Energy, Washington, DC, USA, 2003.
  80. F. G. Simon, V. Biermann, C. Segebade, and M. Hedrich, “Behaviour of uranium in hydroxyapatite-bearing permeable reactive barriers: Investigation using 237U as a radioindicator,” Science of the Total Environment, vol. 326, no. 1–3, pp. 249–256, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. Y. J. Lee, E. J. Elzinga, and R. J. Reeder, “Sorption mechanisms of zinc on hydroxyapatite: systematic uptake studies and EXAFS spectroscopy analysis,” Environmental Science and Technology, vol. 39, no. 11, pp. 4042–4048, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. D. M. Wellman, J. P. Icenhower, and A. T. Owen, “Comparative analysis of soluble phosphate amendments for the remediation of heavy metal contaminants: effect on sediment hydraulic conductivity,” Environmental Chemistry, vol. 3, no. 3, pp. 219–224, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. R. Q. Liu and D. Y. Zhao, “In situ immobilization of Cu(II) in soils using a new class of iron phosphate nanoparticles,” Chemosphere, vol. 68, no. 10, pp. 1867–1876, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. D. M. Wellman, E. M. Pierce, and M. M. Valenta, “Efficacy of soluble sodium tripolyphosphate amendments for the in-situ immobilisation of uranium,” Environmental Chemistry, vol. 4, no. 5, pp. 293–300, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Hwang, W. Ji, B. Kweon, and J. Khim, “The physico-chemical properties and leaching behaviors of phosphatic clay for immobilizing heavy metals,” Chemosphere, vol. 70, no. 6, pp. 1141–1145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. W. R. Berti and S. D. Cunningham, “In-place inactivation of Pb in Pb-contaminated soils,” Environmental Science and Technology, vol. 31, no. 5, pp. 1359–1364, 1997. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Brown, R. Chaney, J. Hallfrisch, J. A. Ryan, and W. R. Berti, “In situ soil treatments to reduce the phyto- and bioavailability of lead, zinc, and cadmium,” Journal of Environmental Quality, vol. 33, no. 2, pp. 522–531, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. M. J. A. Rijkenberg and C. V. Depree, “Heavy metal stabilization in contaminated road-derived sediments,” Science of the Total Environment, vol. 408, no. 5, pp. 1212–1220, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. K. G. Scheckel and J. A. Ryan, “Spectroscopic speciation and quantification of lead in phosphate-amended soils,” Journal of Environmental Quality, vol. 33, no. 4, pp. 1288–1295, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Chrysochoou, D. Dermatas, and D. G. Grubb, “Phosphate application to firing range soils for Pb immobilization: the unclear role of phosphate,” Journal of Hazardous Materials, vol. 144, no. 1-2, pp. 1–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. M. F. Fanizza, H. Yoon, C. Zhang et al., “Pore-scale evaluation of uranyl phosphate precipitation in a model groundwater system,” Water Resources Research, vol. 49, no. 2, pp. 874–890, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. K. L. Nash, M. P. Jensen, and M. A. Schmidt, “Actinide immobilization in the subsurface environment by in-situ treatment with a hydrolytically unstable organophosphorus complexant: uranyl uptake by calcium phytate,” Journal of Alloys and Compounds, vol. 271–273, pp. 257–261, 1998. View at Publisher · View at Google Scholar · View at Scopus
  93. J. C. Seaman, J. M. Hutchison, B. P. Jackson, and V. M. Vulava, “In situ treatment of metals in contaminated soils with phytate,” Journal of Environmental Quality, vol. 32, no. 1, pp. 153–161, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. C. De Stefano, D. Milea, N. Porcino, and S. Sammartano, “Speciation of phytate ion in aqueous solution. Sequestering ability toward mercury(II) cation in NaClaq at different ionic strengths,” Journal of Agricultural and Food Chemistry, vol. 54, no. 4, pp. 1459–1466, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. C. De Stefano, G. Lando, D. Milea, A. Pettignano, and S. Sammartano, “Formation and stability of cadmium(II)/Phytate complexes by different electrochemical techniques. Critical analysis of results,” Journal of Solution Chemistry, vol. 39, no. 2, pp. 179–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Crea, C. De Stefano, D. Milea, and S. Sammartano, “Formation and stability of phytate complexes in solution,” Coordination Chemistry Reviews, vol. 252, no. 10-11, pp. 1108–1120, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. Q. Y. Ma, T. J. Logan, and S. J. Traina, “Lead immobilization from aqueous solutions and contaminated soils using phosphate rocks,” Environmental Science and Technology, vol. 29, no. 4, pp. 1118–1126, 1995. View at Publisher · View at Google Scholar · View at Scopus
  98. W. D. Bostick, R. J. Stevenson, R. J. Jarabek, and J. L. Conca, “Use of apatite and bone char for the removal of soluble radionuclides in authentic and simulated DOE groundwater,” Advances in Environmental Research, vol. 3, pp. 488–498, 1999. View at Google Scholar
  99. M. E. Hodson, E. Valsami-Jones, and J. D. Cotter-Howells, “Bonemeal additions as a remediation treatment for metal contaminated soil,” Environmental Science and Technology, vol. 34, no. 16, pp. 3501–3507, 2000. View at Publisher · View at Google Scholar · View at Scopus
  100. C. C. Fuller, J. R. Bargar, and J. A. Davis, “Molecular-scale characterization of uranium sorption by bone apatite materials for a permeable reactive barrier demonstration,” Environmental Science and Technology, vol. 37, no. 20, pp. 4642–4649, 2003. View at Publisher · View at Google Scholar · View at Scopus
  101. S. B. Chen, Y. G. Zhu, and Y. B. Ma, “The effect of grain size of rock phosphate amendment on metal immobilization in contaminated soils,” Journal of Hazardous Materials, vol. 134, no. 1–3, pp. 74–79, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. J. K. Yoon, X. Cao, and L. Q. Ma, “Application methods affect phosphorus-induced lead immobilization from a contaminated soil,” Journal of Environmental Quality, vol. 36, no. 2, pp. 373–378, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. P. Thakur, R. C. Moore, and G. R. Choppin, “Sorption of U(VI) species on hydroxyapatite,” Radiochimica Acta, vol. 93, no. 7, pp. 385–391, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. S. Raicevic, J. V. Wright, V. Veljkovic, and J. L. Conca, “Theoretical stability assessment of uranyl phosphates and apatites: selection of amendments for in situ remediation of uranium,” Science of the Total Environment, vol. 355, no. 1-3, pp. 13–24, 2006. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Oliva, J. de Pablo, J.-L. Cortina, J. Cama, and C. Ayora, “Removal of cadmium, copper, nickel, cobalt and mercury from water by Apatite II: column experiments,” Journal of Hazardous Materials, vol. 194, pp. 312–323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. W. D. Schecher and D. C. McAvoy, “MINEQL+: a software environment for chemical equilibrium modeling,” Computers, Environment and Urban Systems, vol. 16, no. 1, pp. 65–76, 1992. View at Google Scholar · View at Scopus
  107. R. Guillaumont, T. Fanghänel, J. Fuger et al., “Chemical thermodynamics 5,” in Update on the Chemical Thermodynamics of Uranium, Neptunium, Plutonium, Americium and Technetium, F. J. Mompean, M. Illemassene, C. Domenech-Orti, and K. Ben-Said, Eds., Elsevier, Amsterdam, The Netherlands, 2003. View at Google Scholar
  108. R. Q. Liu and D. Y. Zhao, “Reducing leachability and bioaccessibility of lead in soils using a new class of stabilized iron phosphate nanoparticles,” Water Research, vol. 41, no. 12, pp. 2491–2502, 2007. View at Publisher · View at Google Scholar · View at Scopus
  109. Z. Z. Zhang, M. Y. Li, W. Chen, S. Z. Zhu, N. N. Liu, and L. Zhu, “Immobilization of lead and cadmium from aqueous solution and contaminated sediment using nano-hydroxyapatite,” Environmental Pollution, vol. 158, no. 2, pp. 514–519, 2010. View at Publisher · View at Google Scholar · View at Scopus
  110. E. Navarro, A. Baun, R. Behra et al., “Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi,” Ecotoxicology, vol. 17, no. 5, pp. 372–386, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Motskin, D. M. Wright, K. Muller et al., “Hydroxyapatite nano and microparticles: correlation of particle properties with cytotoxicity and biostability,” Biomaterials, vol. 30, no. 19, pp. 3307–3317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. X. Zhao, S. Ng, B. C. Heng et al., “Cytotoxicity of hydroxyapatite nanoparticles is shape and cell dependent,” Archives of Toxicology, vol. 87, no. 6, pp. 1037–1052, 2013. View at Publisher · View at Google Scholar · View at Scopus
  113. D. Voet and J. G. Voet, Biochemistry, John Wiley & Sons, Hoboken, NJ, USA, 2004.
  114. C. P. Vance, C. Uhde-Stone, and D. L. Allan, “Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource,” New Phytologist, vol. 157, no. 3, pp. 423–447, 2003. View at Publisher · View at Google Scholar · View at Scopus
  115. K. Y. Kim, D. Jordan, and H. B. Krishnan, “Rahnella aquatilis, a bacterium isolated from soybean rhizosphere, can solubilize hydroxyapatite,” FEMS Microbiology Letters, vol. 153, no. 2, pp. 273–277, 1997. View at Publisher · View at Google Scholar · View at Scopus
  116. G. M. Rossolini, S. Schippa, M. L. Riccio, F. Berlutti, L. E. Macaskie, and M. C. Thaller, “Bacterial nonspecific acid phosphohydrolases: physiology, evolution and use as tools in microbial biotechnology,” Cellular and Molecular Life Sciences, vol. 54, no. 8, pp. 833–850, 1998. View at Publisher · View at Google Scholar · View at Scopus
  117. K. Y. Kim, D. Jordan, and H. B. Krishnan, “Expression of genes from Rahnella aquatilis that are necessary for mineral phosphate solubilization in Escherichia coli,” FEMS Microbiology Letters, vol. 159, no. 1, pp. 121–127, 1998. View at Publisher · View at Google Scholar · View at Scopus
  118. M. A. Whitelaw, T. J. Harden, and K. R. Helyar, “Phosphate solubilisation in solution culture by the soil fungus penicillium radicum,” Soil Biology and Biochemistry, vol. 31, no. 5, pp. 655–665, 1999. View at Publisher · View at Google Scholar · View at Scopus
  119. O. A. Vershinina and L. V. Znamenskaya, “The Pho regulons of bacteria,” Microbiology, vol. 71, no. 5, pp. 497–511, 2002. View at Publisher · View at Google Scholar · View at Scopus
  120. F. D. Dakora and D. A. Phillips, “Root exudates as mediators of mineral acquisition in low-nutrient environments,” Plant and Soil, vol. 245, no. 1, pp. 35–47, 2002. View at Publisher · View at Google Scholar · View at Scopus
  121. H. Lambers, M. W. Shane, M. D. Cramer, S. J. Pearse, and E. J. Veneklaas, “Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits,” Annals of Botany, vol. 98, no. 4, pp. 693–713, 2006. View at Publisher · View at Google Scholar · View at Scopus
  122. G. M. Gadd, “Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation,” Mycological Research, vol. 111, no. 1, pp. 3–49, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. M. Ben Farhat, A. Farhat, W. Bejar et al., “Characterization of the mineral phosphate solubilizing activity of Serratia marcescens CTM 50650 isolated from the phosphate mine of Gafsa,” Archives of Microbiology, vol. 191, no. 11, pp. 815–824, 2009. View at Publisher · View at Google Scholar · View at Scopus
  124. S. Uroz, C. Calvaruso, M. P. Turpault et al., “Efficient mineral weathering is a distinctive functional trait of the bacterial genus Collimonas,” Soil Biology & Biochemistry, vol. 41, no. 10, pp. 2178–2186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. A. Kornberg, N. N. Rao, and D. Ault-Riché, “Inorganic polyphosphate: a molecule of many functions,” Annual Review of Biochemistry, vol. 68, pp. 89–125, 1999. View at Publisher · View at Google Scholar · View at Scopus
  126. J. W. McGrath, S. Cleary, A. Mullan, and J. P. Quinn, “Acid-stimulated phosphate uptake by activated sludge microorganisms under aerobic laboratory conditions,” Water Research, vol. 35, no. 18, pp. 4317–4322, 2001. View at Publisher · View at Google Scholar · View at Scopus
  127. M. J. Seufferheld, H. M. Alvarez, and M. E. Farias, “Role of polyphosphates in microbial adaptation to extreme environments,” Applied and Environmental Microbiology, vol. 74, no. 19, pp. 5867–5874, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. T. Shiba, K. Tsutsumi, H. Yano et al., “Inorganic polyphosphate and the induction of rpoS expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 21, pp. 11210–11215, 1997. View at Publisher · View at Google Scholar · View at Scopus
  129. H. Gonzalez and T. E. Jensen, “Nickel sequestering by polyphosphate bodies in Staphylococcus aureus,” Microbios, vol. 93, no. 376, pp. 179–185, 1998. View at Google Scholar · View at Scopus
  130. K. Tsutsumi, M. Munekata, and T. Shiba, “Involvement of inorganic polyphosphate in expression of SOS genes,” Biochimica et Biophysica Acta: Gene Structure and Expression, vol. 1493, no. 1-2, pp. 73–81, 2000. View at Publisher · View at Google Scholar · View at Scopus
  131. P. L. Foster, “Stress-induced mutagenesis in bacteria,” Critical Reviews in Biochemistry and Molecular Biology, vol. 42, pp. 373–397, 2007. View at Google Scholar
  132. L. Andrade, C. N. Keim, M. Farina, and W. C. Pfeiffer, “Zinc detoxification by a cyanobacterium from a metal contaminated bay in Brazil,” Brazilian Archives of Biology and Technology, vol. 47, no. 1, pp. 147–152, 2004. View at Google Scholar · View at Scopus
  133. N. Renninger, R. Knopp, H. Nitsche, D. S. Clark, and J. D. Keasling, “Uranyl precipitation by Pseudomonas aeruginosa via controlled polyphosphate metabolism,” Applied and Environmental Microbiology, vol. 70, no. 12, pp. 7404–7412, 2004. View at Publisher · View at Google Scholar · View at Scopus
  134. M. Kiyono and H. Pan-Hou, “Genetic engineering of bacteria for environmental remediation of mercury,” Journal of Health Science, vol. 52, no. 3, pp. 199–204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  135. F. Remonsellez, A. Orell, and C. A. Jerez, “Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism,” Microbiology, vol. 152, no. 1, pp. 59–66, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. N. Perdrial, N. Liewig, J.-E. Delphin, and F. Elsass, “TEM evidence for intracellular accumulation of lead by bacteria in subsurface environments,” Chemical Geology, vol. 253, no. 3-4, pp. 196–204, 2008. View at Publisher · View at Google Scholar · View at Scopus
  137. T. J. Reilly, G. S. Baron, F. E. Nano, and M. S. Kuhlenschmidt, “Characterization and sequencing of a respiratory burst-inhibiting acid phosphatase from Francisella tularensis,” The Journal of Biological Chemistry, vol. 271, no. 18, pp. 10973–10983, 1996. View at Publisher · View at Google Scholar · View at Scopus
  138. B. L. Wanner, “Phosphorus assimilation and control of the phosphate regulon,” in Escherichia coli and Salmonella, F. C. Neidhardt, R. Curtiss III, and J. L. Ingraham, Eds., vol. 1 of Cellular and Molecular Biology, pp. 1357–1381, ASM Press, Washington, DC, USA, 2nd edition, 1996. View at Google Scholar
  139. A. M. Burroughs, K. N. Allen, D. Dunaway-Mariano, and L. Aravind, “Evolutionary genomics of the HAD superfamily: understanding the structural Adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes,” Journal of Molecular Biology, vol. 361, no. 5, pp. 1003–1034, 2006. View at Publisher · View at Google Scholar · View at Scopus
  140. J. B. Vincent, M. W. Crowder, and B. A. Averill, “Hydrolysis of phosphate monoesters: a biological problem with multiple chemical solutions,” Trends in Biochemical Sciences, vol. 17, no. 3, pp. 105–110, 1992. View at Publisher · View at Google Scholar · View at Scopus
  141. H. G. Hoppe, “Phosphatase activity in the sea,” Hydrobiologia, vol. 493, pp. 187–200, 2003. View at Publisher · View at Google Scholar · View at Scopus
  142. V. N. Anupama, P. N. Amrutha, G. S. Chitra, and B. Krishnakumar, “Phosphatase activity in anaerobic bioreactors for wastewater treatment,” Water Research, vol. 42, no. 10-11, pp. 2796–2802, 2008. View at Publisher · View at Google Scholar · View at Scopus
  143. G. M. Gadd, “Metals, minerals and microbes: geomicrobiology and bioremediation,” Microbiology, vol. 156, no. 3, pp. 609–643, 2010. View at Publisher · View at Google Scholar · View at Scopus
  144. L. E. Macaskie and A. C. R. Dean, “Cadmium accumulation by micro-organisms,” Environmental Technology Letters, vol. 3, no. 2, pp. 49–56, 1982. View at Google Scholar · View at Scopus
  145. L. E. Macaskie and A. C. R. Dean, “Strontium accumulation by immobilized cells of a Citrobacter sp.,” Biotechnology Letters, vol. 7, no. 9, pp. 627–630, 1985. View at Publisher · View at Google Scholar · View at Scopus
  146. B. C. Jeong, P. S. Poole, A. C. Willis, and L. E. Macaskie, “Purification and chacterization of acid-type phosphatases from a heavy- metal-accumulating Citrobacter sp.,” Archives of Microbiology, vol. 169, no. 2, pp. 166–173, 1998. View at Publisher · View at Google Scholar · View at Scopus
  147. M. Paterson-Beedle, L. E. Macaskie, C. H. Lee, J. A. Hriljac, K. Y. Jee, and W. H. Kim, “Utilisation of a hydrogen uranyl phosphate-based ion exchanger supported on a biofilm for the removal of cobalt, strontium and caesium from aqueous solutions,” Hydrometallurgy, vol. 83, no. 1–4, pp. 141–145, 2006. View at Publisher · View at Google Scholar · View at Scopus
  148. R. L. Felts, T. J. Reilly, M. J. Calcutt, and J. J. Tanner, “Cloning, purification and crystallization of Bacillus anthracis class C acid phosphatase,” Acta Crystallographica Section F, vol. 62, no. 7, pp. 705–708, 2006. View at Publisher · View at Google Scholar · View at Scopus
  149. L. G. Powers, H. J. Mills, A. V. Palumbo, C. Zhang, K. Delaney, and P. A. Sobecky, “Introduction of a plasmid-encoded phoA gene for constitutive overproduction of alkaline phosphatase in three subsurface Pseudomonas isolates,” FEMS Microbiology Ecology, vol. 41, no. 2, pp. 115–123, 2002. View at Publisher · View at Google Scholar · View at Scopus
  150. D. Appukuttan, A. S. Rao, and S. K. Apte, “Engineering of Deinococcus radiodurans R1 for bioprecipitation of uranium from dilute nuclear waste,” Applied and Environmental Microbiology, vol. 72, no. 12, pp. 7873–7878, 2006. View at Publisher · View at Google Scholar · View at Scopus
  151. K. S. Nilgiriwala, A. Alahari, A. S. Rao, and S. K. Apte, “Cloning and overexpression of alkaline phosphatase PhoK from Sphingomonas sp. strain BSAR-1 for bioprecipitation of uranium from alkaline solutions,” Applied and Environmental Microbiology, vol. 74, no. 17, pp. 5516–5523, 2008. View at Publisher · View at Google Scholar · View at Scopus
  152. A. Geissler, M. Merroun, G. Geipel, H. Reuther, and S. Selenska-Pobell, “Biogeochemical changes induced in uranium mining waste pile samples by uranyl nitrate treatments under anaerobic conditions,” Geobiology, vol. 7, no. 3, pp. 282–294, 2009. View at Publisher · View at Google Scholar · View at Scopus
  153. M. J. Beazley, R. J. Martinez, S. M. Webb, P. A. Sobecky, and M. Taillefert, “The effect of pH and natural microbial phosphatase activity on the speciation of uranium in subsurface soils,” Geochimica et Cosmochimica Acta, vol. 75, no. 19, pp. 5648–5663, 2011. View at Publisher · View at Google Scholar · View at Scopus
  154. A. L. Neal, K. Lowe, T. L. Daulton, J. Jones-Meehan, and B. J. Little, “Oxidation state of chromium associated with cell surfaces of Shewanella oneidensis during chromate reduction,” Applied Surface Science, vol. 202, no. 3-4, pp. 150–159, 2002. View at Publisher · View at Google Scholar · View at Scopus
  155. P. Pattanapipitpaisal, A. N. Mabbett, J. A. Finlay et al., “Reduction of Cr(VI) and bioaccumulation of chromium by gram positive and gram negative microorganisms not previously exposed to Cr-stress,” Environmental Technology, vol. 23, no. 7, pp. 731–745, 2002. View at Publisher · View at Google Scholar · View at Scopus
  156. C. E. Mire, J. A. Tourjee, W. F. O'Brien, K. V. Ramanujachary, and G. B. Hecht, “Lead precipitation by Vibrio harveyi : evidence for novel quorum-sensing interactions,” Applied and Environmental Microbiology, vol. 70, no. 2, pp. 855–864, 2004. View at Publisher · View at Google Scholar · View at Scopus
  157. M. J. Beazley, R. J. Martinez, P. A. Sobecky, S. M. Webb, and M. Taillefert, “Uranium biomineralization as a result of bacterial phosphatase activity: insights from bacterial isolates from a contaminated subsurface,” Environmental Science & Technology, vol. 41, no. 16, pp. 5701–5707, 2007. View at Publisher · View at Google Scholar · View at Scopus
  158. F. Jroundi, M. L. Merroun, J. M. Arias, A. Rossberg, S. Selenska-Pobell, and M. T. González-Muñoz, “Spectroscopic and microscopic characterization of uranium biomineralization in Myxococcus xanthus,” Geomicrobiology Journal, vol. 24, no. 5, pp. 441–449, 2007. View at Publisher · View at Google Scholar · View at Scopus
  159. J. de Pablo, I. Casas, J. Giménez et al., “The oxidative dissolution mechanism of uranium dioxide. I. The effect of temperature in hydrogen carbonate medium,” Geochimica et Cosmochimica Acta, vol. 63, no. 19-20, pp. 3097–3103, 1999. View at Publisher · View at Google Scholar · View at Scopus
  160. K. T. Finneran, M. E. Housewright, and D. R. Lovley, “Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments,” Environmental Microbiology, vol. 4, no. 9, pp. 510–516, 2002. View at Publisher · View at Google Scholar · View at Scopus
  161. J. K. Fredrickson, J. M. Zachara, D. W. Kennedy et al., “Influence of Mn oxides on the reduction of uranium(VI) by the metal-reducing bacterium Shewanella putrefaciens,” Geochimica et Cosmochimica Acta, vol. 66, no. 18, pp. 3247–3262, 2002. View at Publisher · View at Google Scholar · View at Scopus
  162. C. X. Liu, J. M. Zachara, J. K. Fredrickson, D. W. Kennedy, and A. Dohnalkova, “Modeling the inhibition of the bacterial reduction of U(VI) by β-MnO2(s),” Environmental Science and Technology, vol. 36, no. 7, pp. 1452–1459, 2002. View at Publisher · View at Google Scholar · View at Scopus
  163. J. D. Istok, J. M. Senko, L. R. Krumholz et al., “In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer.,” Environmental Science and Technology, vol. 38, no. 2, pp. 468–475, 2004. View at Publisher · View at Google Scholar · View at Scopus
  164. B. Gu, H. Yan, P. Zhou, D. B. Watson, M. Park, and J. Istok, “Natural humics impact uranium bioreduction and oxidation,” Environmental Science and Technology, vol. 39, no. 14, pp. 5268–5275, 2005. View at Publisher · View at Google Scholar · View at Scopus
  165. J. Wan, T. K. Tokunaga, E. Brodie et al., “Reoxidation of bioreduced uranium under reducing conditions,” Environmental Science and Technology, vol. 39, no. 16, pp. 6162–6169, 2005. View at Publisher · View at Google Scholar · View at Scopus
  166. M. Ginder-Vogel, C. S. Criddle, and S. Fendorf, “Thermodynamic constraints on the oxidation of biogenic UO2 by Fe(III) (Hydr)oxides,” Environmental Science and Technology, vol. 40, no. 11, pp. 3544–3550, 2006. View at Publisher · View at Google Scholar · View at Scopus
  167. J. D. Wall and L. R. Krumholz, “Uranium reduction,” Annual Review of Microbiology, vol. 60, pp. 149–166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  168. H. S. Moon, J. Komlos, and P. R. Jaffé, “Uranium reoxidation in previously bioreduced sediment by dissolved oxygen and nitrate,” Environmental Science and Technology, vol. 41, no. 13, pp. 4587–4592, 2007. View at Publisher · View at Google Scholar · View at Scopus
  169. B. Gu, W.-M. Wu, M. A. Ginder-Vogel et al., “Bioreduction of uranium in a contaminated soil column,” Environmental Science and Technology, vol. 39, no. 13, pp. 4841–4847, 2005. View at Publisher · View at Google Scholar · View at Scopus
  170. W.-M. Wu, J. Carley, T. Gentry et al., “Pilot-scale in situ bioremedation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability,” Environmental Science and Technology, vol. 40, no. 12, pp. 3986–3995, 2006. View at Publisher · View at Google Scholar · View at Scopus
  171. R. S. Oremland and J. F. Stolz, “The ecology of arsenic,” Science, vol. 300, no. 5621, pp. 939–944, 2003. View at Publisher · View at Google Scholar · View at Scopus
  172. R. P. Deo and B. E. Rittmann, “A biogeochemical framework for bioremediation of plutonium(V) in the subsurface environment,” Biodegradation, vol. 23, no. 4, pp. 525–534, 2012. View at Publisher · View at Google Scholar · View at Scopus
  173. R. Finch and T. Murakami, “Systematics and paragenesis of uranium minerals,” in Uranium: Mineralogy, Geochemistry and the Environment, P. C. Burns and R. Finch, Eds., Mineralogical Society of America, Washington, Wash, USA, 1999. View at Google Scholar
  174. E. C. Buck, N. R. Brown, and N. L. Dietz, “Contaminant uranium phases and leaching at the Fernald site in Ohio,” Environmental Science & Technology, vol. 30, no. 1, pp. 81–88, 1996. View at Publisher · View at Google Scholar · View at Scopus
  175. Y. Roh, S. R. Lee, S.-K. Choi, M. P. Elless, and S. Y. Lee, “Physicochemical and mineralogical characterization of uranium-contaminated soils,” Soil and Sediment Contamination, vol. 9, no. 5, pp. 463–486, 2000. View at Publisher · View at Google Scholar · View at Scopus
  176. C. C. Fuller, J. R. Bargar, J. A. Davis, and M. J. Piana, “Mechanisms of uranium interactions with hydroxyapatite: implications for groundwater remediation,” Environmental Science & Technology, vol. 36, no. 2, pp. 158–165, 2002. View at Publisher · View at Google Scholar · View at Scopus
  177. D. M. Wellman, J. N. Glovack, K. Parker, E. L. Richards, and E. M. Pierce, “Sequestration and retention of uranium(VI) in the presence of hydroxylapatite under dynamic geochemical conditions,” Environmental Chemistry, vol. 5, no. 1, pp. 40–50, 2008. View at Publisher · View at Google Scholar · View at Scopus
  178. J. R. Lloyd, P. Yong, and L. E. Macaskie, “Biological reduction and removal of Np(V) by two microorganisms,” Environmental Science & Technology, vol. 34, no. 7, pp. 1297–1301, 2000. View at Publisher · View at Google Scholar · View at Scopus
  179. M. I. Boyanov, K. E. Fletcher, M. J. Kwon et al., “Solution and microbial controls on the formation of reduced U(IV) species,” Environmental Science & Technology, vol. 45, no. 19, pp. 8336–8344, 2011. View at Publisher · View at Google Scholar · View at Scopus
  180. D. K. Newman and J. F. Banfield, “Geomicrobiology: how molecular-scale interactions underpin biogeochemical systems,” Science, vol. 296, no. 5570, pp. 1071–1077, 2002. View at Publisher · View at Google Scholar · View at Scopus
  181. H. L. Ehrlich, “Geomicrobiology: its significance for geology,” Earth Science Reviews, vol. 45, no. 1-2, pp. 45–60, 1998. View at Publisher · View at Google Scholar · View at Scopus
  182. J. Macalady and J. F. Banfield, “Molecular geomicrobiology: genes and geochemical cycling,” Earth and Planetary Science Letters, vol. 209, no. 1-2, pp. 1–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  183. EPA, “Use of monitored natural attenuation at superfund, RCRA corrective action and underground storage tank sites,” OSWER Directive 9200.4-17P, U.S. Environmental Protection Agency, Washington, Wash, USA, 1999. View at Google Scholar
  184. J. Fruchter, “In situ treatment of chromium-contaminated groundwater,” Environmental Science & Technology, vol. 36, no. 23, pp. 464A–472A, 2002. View at Google Scholar · View at Scopus
  185. C. N. Mulligan and R. N. Yong, “Natural attenuation of contaminated soils,” Environment International, vol. 30, no. 4, pp. 587–601, 2004. View at Publisher · View at Google Scholar · View at Scopus
  186. EPA, Monitored Natural Attenuation of Inorganic Contaminants in Ground Water Volume 1—Technical Basis for Assessment, EPA/600/R-07/139, U.S. Environmental Protection Agency, Washington, DC, USA, 2007.
  187. EPA, “Monitored natural attenuation of inorganic contaminants in ground water, Volume 2—Assessment for non-radionuclides including arsenic, cadmium, chromium, copper, lead, nickel, nitrate, perchlorate, and selenium,” EPA/600/R-07/140, Environmental Protection Agency, Washington, DC, USA, 2007.
  188. G. Basnakova and L. E. Macaskie, “Microbially-enhanced chemisorption of Ni2+ ions into biologically-synthesised hydrogen uranyl phosphate (HUP) and selective recovery of concentrated Ni2+ using citrate or chloride ion,” Biotechnology Letters, vol. 23, no. 1, pp. 67–70, 2001. View at Publisher · View at Google Scholar · View at Scopus
  189. J. E. Stubbs, D. C. Elbert, D. R. Veblen, and C. Zhu, “Electron microbeam investigation of uranium-contaminated soils from Oak Ridge, TN, USA,” Environmental Science and Technology, vol. 40, no. 7, pp. 2108–2113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  190. K. R. Salome, S. J. Green, M. J. Beazley, S. M. Webb, J. E. Kostka, and M. Taillefert, “The role of anaerobic respiration in the immobilization of uranium through biomineralization of phosphate minerals,” Geochimica et Cosmochimica Acta, vol. 106, pp. 344–363, 2013. View at Publisher · View at Google Scholar · View at Scopus
  191. M. Fomina, J. M. Charnock, S. Hillier, R. Alvarez, and G. M. Gadd, “Fungal transformations of uranium oxides,” Environmental Microbiology, vol. 9, no. 7, pp. 1696–1710, 2007. View at Publisher · View at Google Scholar · View at Scopus
  192. T. Reitz, M. L. Merroun, A. Rossberg, and S. Selenska-Pobell, “Interactions of Sulfolobus acidocaldarius with uranium,” Radiochimica Acta, vol. 98, no. 5, pp. 249–257, 2010. View at Publisher · View at Google Scholar · View at Scopus
  193. T. Reitz, M. L. Merroun, A. Rossberg, R. Steudtner, and S. Selenska-Pobell, “Bioaccumulation of U(VI) by Sulfolobus acidocaldarius under moderate acidic conditions,” Radiochimica Acta, vol. 99, no. 9, pp. 543–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  194. E. L. Brodie, T. Z. DeSantis, D. C. Joyner et al., “Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation,” Applied and Environmental Microbiology, vol. 72, no. 9, pp. 6288–6298, 2006. View at Publisher · View at Google Scholar · View at Scopus
  195. J. D. Van Nostrand, W.-M. Wu, L. Wu et al., “GeoChip-based analysis of functional microbial communities during the reoxidation of a bioreduced uranium-contaminated aquifer,” Environmental Microbiology, vol. 11, no. 10, pp. 2611–2626, 2009. View at Publisher · View at Google Scholar · View at Scopus
  196. I. Porat, T. A. Vishnivetskaya, J. J. Mosher et al., “Characterization of archaeal community in contaminated and uncontaminated surface stream sediments,” Microbial Ecology, vol. 60, no. 4, pp. 784–795, 2010. View at Publisher · View at Google Scholar · View at Scopus
  197. G. Rastogi, S. Osman, P. A. Vaishampayan, G. L. Andersen, L. D. Stetler, and R. K. Sani, “Microbial diversity in uranium mining-impacted soils as revealed by high-density 16S microarray and clone library,” Microbial Ecology, vol. 59, no. 1, pp. 94–108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  198. T. M. Gihring, G. Zhang, C. C. Brandt et al., “A limited microbial consortium is responsible for extended bioreduction of uranium in a contaminated aquifer,” Applied and Environmental Microbiology, vol. 77, no. 17, pp. 5955–5965, 2011. View at Publisher · View at Google Scholar · View at Scopus
  199. J. D. Van Nostrand, L. Wu, W.-M. Wu et al., “Dynamics of microbial community composition and function during in situ bioremediation of a uranium-contaminated aquifer,” Applied and Environmental Microbiology, vol. 77, no. 11, pp. 3860–3869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  200. K. Katsaveli, D. Vayenas, G. Tsiamis, and K. Bourtzis, “Bacterial diversity in Cr(VI) and Cr(III)-contaminated industrial wastewaters,” Extremophiles, vol. 16, no. 2, pp. 285–296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  201. Y. Liang, J. D. Van Nostrand, L. A. N'Guessan et al., “Microbial functional gene diversity with a shift of subsurface redox conditions during in situ uranium reduction,” Applied and Environmental Microbiology, vol. 78, no. 8, pp. 2966–2972, 2012. View at Publisher · View at Google Scholar · View at Scopus
  202. K. Chourey, S. Nissen, and T. Vishnivetskaya, “Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site,” Proteomics, vol. 13, no. 18-19, pp. 2921–2930, 2013. View at Google Scholar
  203. K. M. Handley, N. C. VerBerkmoes, C. I. Steefel et al., “Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community,” ISME Journal, vol. 7, no. 4, pp. 800–816, 2013. View at Publisher · View at Google Scholar · View at Scopus
  204. S. Kang, J. D. Van Nostrand, H. L. Gough et al., “Functional gene array-based analysis of microbial communities in heavy metals-contaminated lake sediments,” FEMS Microbiology Ecology, vol. 86, pp. 200–214, 2013. View at Publisher · View at Google Scholar · View at Scopus
  205. A. C. Somenahally, J. J. Mosher, T. Yuan et al., “Hexavalent chromium reduction under fermentative conditions with lactate stimulated native microbial communities,” Plos ONE, vol. 8, no. 12, Article ID e83909, 2013. View at Publisher · View at Google Scholar
  206. R. J. Martinez, C. H. Wu, and M. J. Beazley, “Microbial community responses to organophosphate substrate additions in contaminated subsurface sediments,” Plos ONE, vol. 9, no. 6, Article ID e100383, 2014. View at Google Scholar
  207. S. D. Kelly, K. M. Kemner, J. B. Fein et al., “X-ray absorption fine structure determination of pH-dependent U-bacterial cell wall interactions,” Geochimica et Cosmochimica Acta, vol. 66, no. 22, pp. 3855–3871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  208. S. D. Kelly, K. M. Kemner, J. Carley et al., “Speciation of uranium in sediments before and after in situ biostimulation,” Environmental Science & Technology, vol. 42, no. 5, pp. 1558–1564, 2008. View at Publisher · View at Google Scholar · View at Scopus
  209. S. D. Kelly, W.-M. Wu, F. Yang et al., “Uranium transformations in static microcosms,” Environmental Science and Technology, vol. 44, no. 1, pp. 236–242, 2010. View at Publisher · View at Google Scholar · View at Scopus
  210. DOE, “New frontiers in characterizing biological systems: report from the May 2009 workshop,” Tech. Rep. DOE/SC-0121, U.S. Department of Energy Office of Science, Washington, DC, USA, 2009. View at Google Scholar