Potential Impact of Seawater Uranium Extraction on Marine Life

Feb 18, 2016 - Although the oceans contain over 4 billion metric tons of dissolved ..... activities involved with extraction, cleanup, and redeploymen...
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Potential Impact of Seawater Uranium Extraction on Marine Life Jiyeon Park,* Robert T. Jeters, Li-Jung Kuo, Jonathan E. Strivens, Gary A. Gill, Nicholas J. Schlafer, and George T. Bonheyo Marine Science Laboratory, Pacific Northwest National Laboratory, 1529 West Sequim Bay Road, Sequim, Washington 98382, United States ABSTRACT: A variety of adsorbent materials have been developed to extract uranium from seawater as an alternative traditional terrestrial mining. A large-scale deployment of these adsorbents would be necessary to recover useful quantities of uranium, and this raises a number of concerns regarding potential impacts on the surrounding marine environment. Two concerns are whether or not the adsorbent materials are toxic and any potentially harmful effects that may result from depleting uranium or vanadium (also highly concentrated by the adsorbents) from the local environment. To test the potential toxicity of the adsorbent with or without bound metals, Microtox assays were used to test both direct contact toxicity and the toxicity of any leachate in the seawater. The Microtox assay was chosen because it detected nonspecific mechanisms of toxicity. Toxicity was not observed with leachates from any of the 68 adsorbent materials that were tested, but direct contact with some adsorbents at very high adsorbent concentrations exhibited toxicity. These concentrations are, however, very unlikely to be seen in the actual marine deployment. Adsorbents that accumulated uranium and trace metals were also tested for toxicity, and no toxic effect was observed. Biofouling on the adsorbents and in columns or flumes containing the adsorbents also indicates that the adsorbents are not toxic and that there may not be an obvious deleterious effect resulting from removing uranium and vanadium from seawater. An extensive literature search was also performed to examine the potential impact of uranium and vanadium extraction from seawater on marine life using the Pacific Northwest National Laboratory’s (PNNL’s) document analysis tool, IN-SPIRE. Although other potential environmental effects must also be considered, results from both the Microtox assay and the literature search provide preliminary evidence that uranium extraction from seawater could be performed with minimal impact on marine fauna.

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INTRODUCTION Although the oceans contain over 4 billion metric tons of dissolved uranium, the relatively low concentration of uranium in seawater (3.3 ppb)1 requires the development of extraction methods that are highly efficient for this approach to be economically competitive with the traditional terrestrial mining.2,3 A variety of adsorbent materials are currently being explored, such as high surface area polymeric fibers containing amidoxime-based functional ligands that are semiselective for uranium. While advances in adsorbent design may soon make uranium extraction from seawater technically and economically feasible, any significant adverse environment effects could prevent such technology from being used. Either the adsorbents alone, leachates from adsorbents, or the adsorbents with bound metals might be toxic to marine organisms. Therefore, the early identification of toxic or inert behavior is a critical factor to be considered in the selection of materials for further development. The toxicity of adsorbent materials was evaluated using the assay to determine if the supplied adsorbent materials, seawater effluent from uranium extraction columns, as well as adsorbents containing uranium and trace metals have any toxic effects on marine organisms. The Microtox assay measures the luminescence of the bioluminescent marine bacterium Aliivibrio © 2016 American Chemical Society

f ischeri (ATCC 49387), an indicator of metabolism in the organism, after a 30 min4 exposure to a test sample. The Microtox assay is a useful tool to evaluate the toxicity of a wide range of metals5,6 and organic compounds7,8 that are either in liquid or solid phase. In addition, the Microtox assay is lowcost, easy to perform, and has a long history of use for determining toxicity in environmental samples.9−11 Daizel et al.12 evaluated 5 assays, including Microtox, respirometry, nitrification inhibition, ATP luminescence, and enzyme inhibition for use with single toxins, mixed toxicants, and industrial wastes and found the Microtox assay to be the most sensitive, fastest, and most economical. The Advanced Monitoring Systems (AMS) Center that is part of the Environmental Technology Verification (ETV) Program, supported by the U.S. Environmental Protection Agency (EPA), has evaluated, tested, and validated the Microtox assay for assessing various contaminants in water samples. The Special Issue: Uranium in Seawater Received: Revised: Accepted: Published: 4278

September 14, 2015 February 12, 2016 February 18, 2016 February 18, 2016 DOI: 10.1021/acs.iecr.5b03430 Ind. Eng. Chem. Res. 2016, 55, 4278−4284

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Industrial & Engineering Chemistry Research

Seawater Effluent Samples from Flow-through Columns. Adsorbents were prepared and exposed to seawater in columns as described previously.3 Briefly, each adsorbent material was packed inside a column between 5 mm glass beads and glass fiber to stay in place. The columns were either 47 mm diameter perfluoroalkoxy (PFA) Cole-Parmer in-line filter holders or 4−6 in. long by 1 in., internal diameter PVC and polypropylene columns. The adsorbent was exposed to 0.45 μm filtered seawater passing through the column. The temperature of seawater was set at 20 °C. The seawater flow rate was adjusted to 250−300 mL/min. Columns were wrapped in aluminum foil to avoid exposure to light during uranium capacity testing. Seawater effluent samples were collected in sterile 50 mL centrifuge tubes at three different time points (1 h, 1 day, and 1 week) following the start of the experiments to determine if exposure time might affect the toxicity: i.e., was there an initial release of unbound solid or soluble toxic material. Braided Adsorbent Samples from a Flume. The braided ORNL AI8 adsorbent was exposed to 150 μm filtered seawater in a dark flume kept out of light for 42 days, and the braid samples were collected at 6 different time points (0 time, 7 days, 14 days, 21 days, 28 days, and 42 days). The 0 time samples were collected after adsorbents were exposed to seawater for 2 min. The dark flume was designed to avoid exposure to light, which leads to increased biofouling on the adsorbents and on the walls of the flume. Adsorbent samples were dried on a heating block (80 °C, overnight) and weighed prior to the Microtox assay. In-Spire. IN-SPIRE is a visual document analysis tool developed by the Pacific Northwest National Laboratory (PNNL). It is a tool that allows analysis of large volumes of data, such as literature searches, to ascertain relationships and trends and display the information in a variety of formats, including graphical displays of publications by year, country, institution, or author; key word usage; or as 3-dimensional heat maps that organize documents according to subtopics. Critically for this study, IN-SPIRE documents the search terms and their relationships to the acquired data. In this paper, data was collected from PubMed, an online scientific search engine that contains 23 million citations. A list of terms was searched, and the resulting documents were complied and analyzed through the IN-SPIRE program. A total of 1,466 uranium documents and 1,064 vanadium documents were analyzed by IN-SPIRE in two separate analyses.

Microtox assay has also been used by the U.S. Geological Survey (USGS) and National Oceanic and Atmospheric Administration (NOAA) to assay sediments from Delaware Bay and surrounding areas for toxicity.13,14 In addition to potential toxicity of uranium adsorbent materials, the removal of uranium and vanadium from seawater in large-scale might have unforeseen adverse effects on marine life. With the current uranium adsorbent materials, vanadium is the predominant metal adsorbed. This is a potential concern since some marine inhabitants utilize vanadium, but there is little evidence that organisms require vanadium or uranium as an essential element. For example, neither element is included in any of the commonly used growth media recipes for prokaryotes or microeukaryotes. An exhaustive literature search was performed to identify any evidence that either element might have an essential role in supporting life or some metabolic function. As it is difficult to prove negative results, the IN-SPIRE, a visual document analysis tool developed by Pacific Northwest National Laboratory (PNNL), was used to document the thoroughness of the search and the acquired results. Uranium and vanadium article searches were done to identify potential risks posed to the marine environment by uranium mining from seawater. The work presented herein addresses questions of (1) whether the uranium adsorbent materials and their leachates are toxic to marine organisms, (2) whether adsorbents with bound and concentrated metals might be particularly toxic, and(3) whether extraction of uranium and vanadium would affect the marine environment.

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EXPERIMENTAL METHODS Microtox Assays. Aliivibrio fischeri culture was grown overnight in ALNa Broth4 at 22 °C with vigorous shaking. The overnight culture was used to inoculate 10 mL of ALNa broth, and the fresh culture was incubated with vigorous shaking at 22 °C. Cells were grown until the optical density at 590 nm (OD590) reached 0.25. Cells were harvested by centrifugation at 4150 rpm for 5 min followed by washing with 10 mL of 3% NaCl; pH 7.0. Cells were then resuspended in 10 mL of 3% NaCl at pH 7.0. The cell suspension was mixed with test materials for 30 min, and the luminescence was measured using a Synergy HT microplate reader (Biotek, VT, USA). The Decrease in Bacterial Luminescence (INH%). The decrease in bacterial luminescence (INH %) was calculated as previously described.15 If the luminescence decreased by more than 50% after exposure to sample materials for 30 min,4 the concentration of toxicant is designated as the effective concentration (EC50).15 Values obtained with a cells only control sample (cell suspension in 3% NaCl or 0.45 μm filtered seawater) were set as 100%, and the luminescence of each test sample was represented as a percentage of the control value. ZnSO416 was used as a control toxicant to validate the Microtox assay results. Adsorbents. Adsorbent materials were provided by several different laboratories participating in the U.S. Department of Energy’s Fuel Resources Campaign and in a parallel program in China. For some experiments, the ORNL AI8 adsorbent was used. This material entails a polyethylene support fiber and amidoxime ligands. The toxicity assays did not directly discriminate between toxic effects of the ligand chemistry and toxic effects of the support material, but comparisons of materials using similar supports with different ligands may be used to rule out support material toxicity.

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RESULTS AND DISCUSSION Toxicity Evaluation of Adsorbent Materials and Seawater Effluent. Supplied adsorbent materials were tested for the direct contact toxicity using increasing concentrations of adsorbent to find the EC50 value. Due to the fact that only a limited number of adsorbent materials were made available, only 10 samples were tested, and hence the results from direct contact toxicity testing should be considered preliminary. Results are shown in Table 1. Five out of ten samples were shown to be toxic at very high concentrations (equal to or greater than 0.3125 mg/mL). It is important to note that these are exceptionally high concentrations and that during field deployment the adsorbent materials will be exposed in the marine environment at ppb or lower levels. In order to determine whether adsorbent materials or chemistry leaching into the surrounding seawater could have toxic effects on marine organisms, time-course experiments 4279

DOI: 10.1021/acs.iecr.5b03430 Ind. Eng. Chem. Res. 2016, 55, 4278−4284

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none observed up to 2.5 mg/mL none observed up to 2.5 mg/mL

a EC50 is the effective concentration of the test sample that reduces luminescence from bacteria by 50%. 5 out of 10 samples tested had EC50 at very high concentrations. YF130226C was provided as a suspension of liquid. Other adsorbents were solid materials.

4280

source

Table 2. List of Adsorbent Samples Tested for Leachate Toxicitya

adsorbent

were performed using seawater effluent samples collected after contact with 68 different adsorbent materials provided by several laboratories engaged in the US-DOE or Chinese programs (Table 2). Each seawater effluent sample was collected from the outflow of a column holding a given adsorbent sample as that sample was undergoing testing to determine uranium uptake kinetics and capacity. Each effluent sample was tested individually: i.e., samples were not pooled, and therefore each adsorbent was tested individually. Effluent samples were collected at three different time points: 1 h, 1 day, and 1 week after seawater began to flow over the adsorbent materials in the uranium uptake columns. The Microtox assay was performed over a range of effluent concentrations: increasing amounts of seawater effluent were added to a cell suspension up to a maximum of 75% v/v effluent sample/cell suspension. A 25% v/v minimum volume of Aliivibrio f ischeri cell suspension is required to measure the luminescence. Four concentrations were used for each effluent sample: 5%, 25%, 50%, and 75% v/v, and three independent tests were done for each concentration. In summary, no toxicity was observed with seawater effluent that was in contact with any of the 68 different adsorbent materials (Table 2). Thus, toxicity via adsorbent leaching can be excluded as a potential harmful source for the marine environment. Another potential source of toxicity may come from the accumulation of metals on the adsorbents. Metals that are toxic can inhibit growth or have other deleterious health effects. As adsorbent materials are exposed to seawater during the uranium mining process, the concentration of various metals on their surface will increase, surpassing the concentration levels found in the surrounding seawater (Table 3). This may result in creating a potentially toxic surface or surface associated microenvironment. In order to address this concern, experiments were designed to test adsorbent materials that had accumulated uranium and other metals. Five different concentrations (mg adsorbent/ml A. f ischeri cell suspension) of each sample were analyzed using the Microtox assay. None of the samples exhibited EC50 toxicity, even at the very high metal saturated adsorbent concentrations (Figure 1). However, adsorbents that had high concentrations of bound metals up to

68 adsorbent materials from 5 different sources were tested for leachate toxicity. Seawater effluent samples that were in contact of adsorbent materials in columns were collected at three different time points (1 h, 1 day, and 1 week) and tested up to 75% v/v. All samples were shown not to have toxic effects.

0.3125 mg/mL

a

Chinese Academy of Science

UHMWPE-g-PAPA-co-PAO 1, UHMWPE-g-PAPA-co-PAO 2, UHMWPE-g-PAPA-co-PAO 3, UHMWPE-g-PAPA-co-PAO 4

MC-phosphate UHMWPE-g-PAPA-coPAO 1 UHMWPE-g-PAPA-coPAO 2 UHMWPE-g-PAPA-coPAO 3 UHMWPE-g-PAPA-coPAO 4

University of North Carolina

B2MP-G-169, B2MP-G-180, B2MP-G-182, B2MP-G-184, B2MP-G-185, B2MP-G-186, recycled B2MP-CT-126

MC-precursor

source ORNL

RJ-02-76-CUNY, RJ-03-66-CUNY

YF130226C CA-4139 CA-4149

EC50 none observed up to 25% v/v 25 mg/mL 1.1 mg/mL none observed up to 6.4 mg/mL none observed up to 10 mg/mL 2.5 mg/mL 0.625 mg/mL

University of Alabama The City University of New York University of Maryland Chinese Academy of Science

adsorbent YF130313C

ORNL

Table 1. Direct Contact Toxicitya

JG159a, JG159b, JG164a, JG192, KMS-2, TSU-27, TSU-39C, TSU-39D, TSU-39E, TSU-45H40, 38H26, 11-651H75C, 11-105, 11-117, 11-119, YF140115A-NH20H, AFL, AF3 RMCJ, AF8 RMCJ, AF160-2 RMCJ, AF1FR2 RMCJ, AF1FR3 RMCJ, AF1B160-5PPI, AF1B16-TOW, AF3, AF1B7-5PPI, AF1B17-25PPI, AF1B17-2-5PPI, AF1B17-2-25PPI, AF1FR2, AF1FR3, AF1L1R1, AF1L1R2, AF1L1R3, AF1L2R1, 2T8 RMCJ, AF1L2R1(Fiber), AF1L2R2(Fiber), AF1L2R3(Fiber), AI8L1R1, AI8L1R2, AI8L2R1, AI8B16-TOW, AI8B16-5PPI, AI8L2R2, AI8L1R3, AI8L2R3, AI8FR2, AI8FR3, AI8B17-TOW, AI8B17-5PPI, AI8B17-25PPI AO-chitin mat, DA-chitin mat, SS-chitin mat

Industrial & Engineering Chemistry Research

DOI: 10.1021/acs.iecr.5b03430 Ind. Eng. Chem. Res. 2016, 55, 4278−4284

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organism growth (data not shown). Vanadium and uranium are also not identified as essential elements for growth and are not included in any of the typical growth media used for prokaryotes, eukaryotes, or archaea. To examine the potential biological effects caused by the removal of uranium and vanadium further, an extensive search on peer-reviewed literature was completed to better understand the role(s) of uranium and vanadium in biological systems. The IN-SPIRE software was used to examine and characterize the results. Graphic depictions of the results from uranium and vanadium article searches are shown in Figure 2.

Table 3. Concentration of Various Metals on the AF1 Adsorbent Following a 56-Day Exposure in Seawatera element

concn (μg/g)

concn (g/kg)

U Ca Co Cr Cu Fe Mg Mn Na Ni Sr Ti V Zn

3495 13707 20.9 13.2 529 883 15810 13.9 1630 356 114 62.0 9592 1195

3.49 13.71 0.02 0.01 0.53 0.88 15.81 0.01 1.63 0.36 0.11 0.06 9.59 1.20

a

Adsorbent materials such as AF1 (polyethylene support with amidoxime ligands) concentrate a variety of metals on their surface. The table above shows the concentration of metals following a 56-day exposure relative to the mean oceanic concentration of the metals.

Figure 2. Visual representation of the grouping of the 3,757 documents presented in Theme View Classic. Each peak represents a group of related journal articles retrieved from PubMed searches using the terms listed above.

There are not many publications that show the direct use of uranium for biological purposes. In bioremediation, bacteria can utilize uranium for respiration under certain conditions; often this requires feeding the bacteria an exogenous carbon source that drives the reaction.17,18 Certain fungi have also been found to interact with trees to allow the absorption of uranium into roots;19 plants are also capable of accumulating uranium naturally.20,21 Yet, the utilization of uranium seems to be a subsidiary need for the host organism and not essential for life. In contrast to uranium, vanadium, appears to have a much larger function in biological systems. Vanadium can also be utilized in bacterial respiration, similar to that of uranium;22 in addition, there are examples of proteins that have vanadium ion cofactors.23 Furthermore, there are organisms that directly accumulate vanadium. Tunicates (a marine invertebrate)24,25 and ascidians (sea squirts) 26 of the phylum chordate concentrate and store vanadium in specialized compartments called vacuoles. However, little is known for the function of this accumulation. Vanadium may be used for biodefense.24 Vanadium has also been shown to be a trace element that encourages the growth of marine algae. The exact mechanism of how this works is not understood, but addition of vanadium to axenic grown lab cultures resulted in a 400% increase in dry weight of the brown alga Fucus spiralis.27 However, no evidence was found in the literature review that vanadium is essential for the growth of any species. Utilization of Uranium/Vanadium as an Electron Acceptor. The use of metals as a terminal electron acceptor is well documented in the terrestrial environment. Micro-

Figure 1. Toxicity testing of adsorbent that accumulated uranium and trace metals. Braided adsorbent material that was exposed to partially filtered seawater and accumulated uranium and trace metal was tested for toxicity using the Microtox assay. Samples collected at each time point were tested at 5 different concentrations, and the luminescence was measured. The luminescence value obtained from cells only samples was set to 100%, and the value obtained from each adsorbent sample was represented as a percentage of the cells only value. The experiments were done in triplicate. Mean values are shown, and standard deviations are indicated as error bars.

2.5 mg/mL did display some levels of toxicity although they did not reach the EC50 level (Figure 1). Therefore, while the presently achievable metal capacity on available adsorbents may not be particularly toxic, this suggests that as adsorbent capacities improve, there is some potential for EC50 level toxicity due to the accumulation of metals. Biological Roles of Uranium and Vanadium. The previous section shows that adsorbents placed in seawater are unlikely to add toxins or concentrate metals in a manner that would harm the surrounding marine environment. However, it may be possible that large-scale operations could deplete the available uranium or vanadium from an environment and thus cause harm to organisms or processes dependent upon those elements. Closed-system tests in which diatoms and other microorganisms were cultured in the presence of sufficient quantities of fibers to remove all uranium and vanadium from the culture medium did not show any negative effects on 4281

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Industrial & Engineering Chemistry Research organisms such as Geobacter are able to use uranium along with the metals Fe(III), Co(III), Cr(VI), and Mn(IV)28−30 as a terminal electron acceptor in cellular respiration. Some environmental remediation strategies utilize microorganisms to reduce soluble uranium(VI) to insoluble uranium(IV), which helps to reduce the chance of uranium migrating into watersheds.31 This conversion process does happen naturally, albeit, at a relatively slow pace. Therefore, remediation sites typically add acetate or other carbon sources32 (electron donors) to the soil to dramatically speed up the utilization and conversion of uranium in the terrestrial environment.32 Microorganisms have also been shown to utilize vanadium as a terminal electron acceptor. Shewanella oneidensis has been shown to reduce sodium metavanadate when feed lactate33 as a carbon source. In the absence of uranium and vanadium as a terminal electron acceptor, Geobacter, Shewanella, and other microbial species can utilize alternate metals to maintain cellular respiration.31 This is due to the plasticity of their metabolic pathways. Thus, removal of uranium and/or vanadium would be expected to have a minimal impact on these or similar metal reducing organisms. Metalloproteins. There are a large number of proteins that contain metal ion cofactors.34 These metalloproteins have multifaceted functions in cells, such as enzymatic activity, transport or storage, and signal transduction. Hemoglobin is a well-known example of a metalloprotein that features a central iron core. In addition to iron, metalloproteins that utilize several different species of metal ion cofactors, such as cadmium, cobalt, copper, magnesium,35 manganese,36 molybdenum,37 nickel,25 selenium, and vanadium,38,39 have been found. However, there is no known protein that contains uranium as an ion cofactor. Therefore, removal of uranium from seawater would not appear to have an impact on metalloprotein production in a marine or terrestrial organism. As noted above, there are metalloproteins that utilize vanadium. One example is a class of nitrogenase enzymes that fix nitrogen gas to ammonia and which have a vanadium cofactor; for example, the photosynthetic microorganism Rhodoseudonomas palustris40 has three isozymes and one of them has a vanadium cofactor. The other two isozymes have a molybdenum and an iron cofactor.40 Therefore, this organism depends on vanadium for its survival. A second example is a group of vanadium bromoperoxidases that carry out bromination in algae;41 fungi and bacteria are carried out by the metalloprotein vanadium bromoperoxidase.42,43 Distribution of Uranium and Vanadium in Seawater. An indirect way to assess whether uranium is utilized in seawater for biological activity is to check its distribution in seawater.44 Elements in seawater that are utilized by marine organisms (e.g., Si, Fe, Cu, Zn) tend to have varying concentrations throughout the water column and in different locations throughout the ocean. These “nutrient like elements”44 are utilized by plankton and other marine organisms that are more concentrated in shallow or surface water. For instance, the concentration of silicon (Si) in ocean seawater increases with depth as a consequence of more rapid biological incorporation at the surface. Diatoms utilize silicon to construct their cell walls; however, they also need to be near the oceans surface to harness the energy of sunlight. Similarly, siliceous radiolarians that may feed on diatoms are also located in the uppermost hundreds of meters in the ocean.

In contrast to Si, the distribution of uranium throughout the seawater column is uniform. This pattern is not characteristic of bioutilization; changes in concentrations of uranium are only proportional to salinity. Monterey Bay Aquarium Research Institute (MBARI) uranium distribution concentration maps show a U concentration of ∼14 nmol/kg at the oceans surface and at 5000 m depth. MBARI classifies this distribution pattern as a “conservative element”, which is not indicative of biological utilization.44 The vertical profile of vanadium is a hybrid of the “nutrient like elements” and “conservative element” distribution patterns. Vanadium shows some depletion at the surface water but less than that of Si.44 This suggests that there is some amount of bioutilization occurring with vanadium, albeit at a lesser rate. This mixed distribution pattern for vanadium, unfortunately, does not fit neatly into any of the currently defined definitions for distribution profiles. MBARI distribution maps suggest that vanadium is being utilized for biological function only at the uppermost portion of the oceans surface, in contrast to silicon that is biologically utilized to greater depths. Therefore, it can be assumed that adsorbent materials deployed below ocean depths of >500 m (Pacific) would have minimal impact on marine fauna that utilize vanadium. Uranium Replenishment: from Rivers to Oceans. If the projected uranium extraction from seawater by adsorbent technology is lower than the amount of uranium returned each year to the ocean from river runoff, then any potential risks to marine life can be minimal. The U.S. Energy Information Administration (EIA)45 reported 4,807,709 pounds of mined U3O5 from mines in Wyoming, Nebraska, Texas, and Utah in 2013, and it is approximately 10% of the required uranium46 for U.S. nuclear reactors. The estimated contribution of uranium to the ocean from river runoff is 15.7−31.4 million pounds,47 which is a larger amount than what is currently contributed from U.S. mines. Thus, the U.S. could meet its yearly 10% input and still be under the natural uranium replenishment rates for oceans. No data could be found at this point to assess the contribution of uranium to oceans from the atmosphere and to determine the influx of vanadium from the atmosphere and river runoff.

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CONCLUSION A large-scale ocean resource extraction program could have many effects on the environment. The presently envisioned “artificial kelp” model of a large benthic-anchored field of adsorbent may introduce toxins (from the adsorbent or extraction process); remove nutrients; disturb the benthic environment; introduce structure that would attract macrofauna including fish, birds, marine mammals, and thus human activity; result in entanglement of macrofauna; alter local currents and sediment transport; and result in disturbances due to the surface activities involved with extraction, cleanup, and redeployment of the adsorbents. In this study, we examined two potential issues: toxicity and whether removal of uranium and a dominant byproduct of extraction, vanadium, could have a harmful impact. Three routes of toxicity were considered: contact toxicity between organisms and the adsorbent surfaces, leachates, and high concentrations of metals accumulating on the adsorbents. A diverse range of natural and synthetic materials is currently under development for use as adsorbent support material and ligand chemistry. Early identification of adsorbent materials that may have potentially toxic and deleterious effects on marine 4282

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organisms is critical during the early stages of development for use as adsorbent support material and ligand chemistry. Early identification of adsorbent materials that may have potentially toxic and deleterious effects on marine organisms is critical during the early stages of development to prevent future problems, allow for concurrent development of mitigation strategies, and ensure an efficient and economical development program. To facilitate this process, adsorbent materials, adsorbents that had accumulated uranium and trace metals, and seawater effluent samples were tested for toxicity. It was found that all were not toxic at ppm levels. A few adsorbent materials were determined to be toxic at very high concentrations (ppt); however, it is highly unlikely that these concentrations would be seen in the actual marine environment under deployment conditions. Biofouling on the samples (reviewed in a separate paper in this issue) provides additional empirical evidence that the adsorbents are not particularly toxic. It must be noted that the toxicity assays used do not necessarily account for potential bioaccumulative effects or effects that may be specific to eukaryotes. Concern that the mass removal of uranium from seawater could have a deleterious effect on marine life had been raised at review program meetings of the U.S. DOE-NE Fuel Campaign. While uranium is not recognized as an essential nutrient and is not included in growth media recipes, an extensive literature has an identified role in any living process. The literature search found limited use of uranium by some organisms but only as a nonessential alternative electron acceptor. Further analysis comparing U.S. energy demands for uranium with ocean resource replenishment from rivers determined that meeting the demand of just the U.S. nuclear energy power industry would outpace marine replenishment by the world’s rivers. However, calculations for other potentially larger inputs (e.g., mid ocean ridges, windblown dust or sand) could not be made at this time. Removal of vanadium from seawater, a byproduct of uranium removal, may need to be investigated more comprehensively before a conclusion can be made about the potential biological impact. Vanadium ions are utilized by certain metalloproteins and are actively concentrated and incorporated into marine organisms such as tunicates for unknown reasons or functions. Thus, there is an established link between biological systems and vanadium in the marine environment. However, the direct impact on biological systems is unclear, and we found no reports of vanadium being an essential element. Further investigation of the marine organisms that utilize vanadium may provide new insights into the role of this element; additionally more information on rate of vanadium removal and replenishment rate for oceans is required. Toxicity of the adsorbents and nutrient depletion do not appear to be problematic, especially when compared with the environmental challenges created by terrestrial mining. Additional research and planning will be needed to ensure that other potential impacts to marine life not examined in this study can be mitigated. Comparisons and lessons learned may be possible with aspects of aquaculture; the shipping industry; offshore wind, tidal, and wave energy; and with offshore oil and gas drilling.

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AUTHOR INFORMATION

Corresponding Author

*Phone: 360-582-2528. Fax: 360-681-4559. E-mail: Jiyeon. [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the U.S. Department of Energy under Contract DE-AC05-76RL01830.

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ABBREVIATIONS MBARI = Monterey Bay Aquarium Research Institute MSL = Marine Science Laboratory PNNL = Pacific Northwest National Laboratory ORNL = Oak Ridge National Laboratory REFERENCES

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