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Siderophore-Mediated Chemistry and Microbial Uptake of Plutonium

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Siderophore-Mediated Chemistry and Microbial Uptake of Plutonium Chemical Interactions of Actinides in the Environment Siderophore-Mediated Chemistry and Microbial Uptake of Plutonium Mary P. Neu etal ions can interact with plutonium by siderophore uptake mech- crystal structures of the free ligand, the microorganisms via a range of anisms. We have focused on two tri.- Fe(III) complex, and the Pu(IV)-DFO Mmechanisms. For example, hydroxamate desferrioxamine (DFO) complex have interesting similarities. metals can sorb directly to an organisms’ siderophores—desferrioxamine E As seen in Figure 2, the DFE occupies cell wall, or can react with microbal (DFE) and desferrioxamine B (DFB)— approximately one-half of the plutonium byproducts, such as extracellular because they are the most-well studied coordination sphere. Three water mole- polymers. A classic system of microbial- and are readily available. cules bind to the plutonium in the metal interaction involves low molecular We have prepared and structurally remaining space. The polytopal geometry weight organic ligands (siderophores) characterized the first plutonium- of the plutonium coordination sphere is which are excreted and used by plants siderophore complex, a slightly distorted tricapped trigonal and microbes to acquire iron. Al(H2O)6[Pu(DFE)(H2O)3]2(CF3SO3)5 prism; the three bound waters and three All microorganisms, except the • 14H2O (Neu et al. 2000). In fact, our oximate oxygens form trigonal planes Lactobacilli, have nutritional require- work is the first structural characteriza- while the three carbonyl oxygens cap ments for Fe(III) that are not met in tion of any plutonium biomolecule. the prismatic faces. aqueous aerobic environments. Under (This complex also contains the first Ruggerio et al. (2000) found that those conditions, Fe(III) has a low solu- verified nine-coordinate Pu4+ ion.) X-ray Pu(IV)-DFO is thermodynamically the bility (at neutral pH, typical concentra- crystallographic data reveal that the most stable complex among all the tions are about 10–18 molar) so that its possible Pu-DFO complexes: regardless bioavailability it limited. In order to O of the initial state of the plutonium, acquire sufficient iron, bacteria synthe- DFE eventually the Pu(IV)-DFO complex size and secrete siderophores that can N HN forms. If Pu(III) is present initially, it is chelate Fe(III) and carry it into the cell HO O rapidly oxidized by DFO to Pu(IV). NH via specific high-affinity uptake recep- Plutonium(V) and Pu(VI) are reduced O O HO tors. The siderophores are typically N to Pu(IV). At neutral pH and higher, multidentate, oxygen-donor ligands that OH O the reduction to Pu(IV) is instanta- N usually have hydroxamate, catecholate, H neous. Under acidic conditions, Pu(VI) or carboxylate moieties. Although they N is rapidly reduced to Pu(V), followed are designed to have an extremely high O by a slow reduction to Pu(IV), with the affinity for Fe+3, siderophores can bind rate dependent on the pH and the DFO other “hard” ions, such as Al(III), concentration. Stoichiometric titration Zn(II), Ga(III), Cr(III),, and, Pu(III,IV). DFB O of Pu(VI) into a DFO solution showed (Hard metal ions have high charge to that up to 12 equivalents of plutonium N HN ionic radius ratios and form strong O could be reduced per DFO, showing NH HO inner sphere complexes with ligands O that DFO is a powerful reductant for O containing “hard” donor atoms, such HO Pu(VI). In contrast, U(VI)-DFO is inert as oxygen.) OH N to reduction. N O We are examining the redox and The formation constant, β, for the NH CH coordination chemistry of plutonium 2 3 Pu(IV)-DFO complex formed at neutral with siderophores in order to under- pH has been estimated to be extremely stand how they could affect actinide Figure 1. Hydroxamate Siderophores high, log β = 30.8, for DFB (Jarvis, et biogeochemistry. We have investigated The chemical structures of two desfer- al., 1991). That constant is higher than the ability of hydroxamate siderophores rioxamine siderophores are shown above; those known for many organic chela- to coordinate Pu(IV) and solubilize the the linear trihydroxamate produced by S. tors, such as EDTA, citrate, and tiron. Pu(IV) solid, Pu(OH)4(s), at neutral pH, pilosus, Desferrioxamine B (DFB), and the High complex-formation constants are and have studied the potential for com- cyclic trihydroxamate produced by P. generally equated with effective solubi- mon soil aerobes to interact with stutzeri., Desferrioxamine E (DFE). lization of the metal ion by the ligand. 416 Los Alamos Science Number 26 2000 Chemical Interactions of Actinides in the Environment (c) Figure 2. Sidereophore Complexation (a) (b) (a) A space filling model of DFE.* (b) Fe- DFE complex.** A twist of the carbon backbone allows the three oximate oxygens and the three carbonyl oxygens to form a “cavity” that securely holds the Fe3+ ion. (c) The Pu-DFE complex is struc- Pu4+ turally similar to Fe-DFE. The large Pu4+ Fe3+ Oximate oxygen ion protudes slightly from the cavity. Three Carbonyl oxygen H O water molecules remain bound to the ion. 2 *Van der Helm, D., and M. Poling. 1976. J. Am. Chem. Soc. 98: 82. **Hossain, M. B., D. van der Helm, and M. Poling. 1983. Acta Cryst. B 39: 258. However, the DFO siderophores are far two orders of magnitude lower than Further Reading less effective at solubilizing Pu(OH)4(s) with iron and exhibits a different time in buffered neutral solution compared dependence. Whereas iron uptake is Cleveland, J. M. 1979. The Chemistry of to the organic chelators, even though fastest at the beginning, generally slow- Plutonium, La Grange Park, Illinois: American Nuclear Society. the latter have lower Pu(IV) complex- ing and leveling out to approximately formation constants (Cleveland, 1991). 100 nanomoles per milligram of bacte- Jarvis, N. V. and R. D. Hancock, 1991: Inorg. Pu(IV) hydroxide can be slowly solubi- ria after 1 hr, plutonium uptake increases Chim. Acta, 182: 229. lized by EDTA at a rate of approxi- linearly until it reaches a peak rate of µ µ John, S. G., C. E. Ruggiero, M. P. Neu, et al. mately 1.1 moles per day ( mol/day), 25 nanomoles per milligram of bacteria Submitted to J. Am. Chem. Soc. Los Alamos and by citrate and tiron at rates of 0.2 after 10 hours. National Laboratory document µmol/day, and 0.1 µmol/day, respec- We have examined competition LA-UR 00-1879. tively. In contrast, the rates of solubi- between Fe-DFB and Pu-DFB uptake lization by DFE and DFB are 50 to 500 by adding different quantities of the Neu M. P., J. H. Matonic, C. E. Ruggiero, and B. L. Scott. 2000: Angew. Chem. Int. Ed. 39: times slower than EDTA. Additionally, metal complexes at varying times. We 1442. EDTA solubilization of Pu(OH)4(s) are currently determining the location of was 10 times slower after pre-treating iron and plutonium on and within the Powell, P. E., G. R. Cline, C. P. P. Reid, and the plutonium with DFB. These cell by using various chemical treat- P. J. Szanislo, 1980: Nature 287: 833. surprising results suggest that the DFO ments of the cells. Our results indicate Ruggiero, C. E., M. P. Neu, et al. Submitted to siderophores are passivating the surface differences in recognition, uptake, and Inorg. Chem. Los Alamos National Laboratory of the Pu(IV) solid and inhibiting final location of the iron and plutonium. document LA-UR 00-1878 solubilization. The Fe-DFB complex is rapidly recog- We also found that DFB can mediate nized by the uptake channel receptors plutonium association with bacteria and is translocated into the cell interior. (John et al. 2000). As an example, the While the Pu-DFB complex appears to Mary Neu earned B.S. degrees in math and soil isolate Aureobacterium flavescens be recognized by the same binding chemistry and graduated magna cum laude from (JG-9) is a siderophore auxotroph, site(s) with approximately the same the University of Alaska, where she was named producing no siderophore of its own affiinity, it is only slowly transported the Outstanding Student in the Physical Sciences in 1986. She received but requiring one to obtain iron. We across the cell membrane into the interior. a Ph. D. in inorganic verified that all iron and plutonium Hydroxamate siderophores are natu- and nuclear chemistry uptake by A. flavescens is strictly asso- rally present in the environment (Powel from the University of ciated with the added siderophore DFB, et al. 1980). They have a high binding California at Berkeley that is, no uptake occurs without its affinity for Pu(IV), a large reducing in 1993 under the direc- tion of Professors Dar- addition. Uptake of Fe-DFB or Pu-DFB capacity for Pu(VI) and Pu(V), and leane Hoffman and also needed living, metabolically active they inhibit the solubilization of pluto- Ken Raymond. After a bacteria; heat-killed or metabolically nium solids. Our recent work shows year as a University of inhibited cells showed little association that Pu-DFO complexes are recognized California post-doctoral research fellow at Los Alamos, she joined the with the Fe-DFB or Pu-DFB complex. by microbial metal-siderophore binding technical staff in 1995. Mary currently directs These results points to similar energy- sites and may be taken into cells. and performs research in the Actinide, Catalysis dependant uptake processes by which These varied and dynamic interactions and Separations Chemistry group in the Chemistry, the iron and plutonium are transported suggest that these strong metal chela- Science, and Technology Division. Her areas of interest include inorganic, environmental, to the cell interior.
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