Uranium association with halophilic and non-halophilic bacteria and archaea

Abstract

We determined the association of uranium with bacteria isolated from the Waste Isolation Pilot Plant (WIPP), Carlsbad, New Mexico, and compared this with known strains of halophilic and non-halophilic bacteria and archaea. Examination of the cultures by transmission electron microscopy (TEM) and energy dispersive X-ray spectroscopy (EDS) showed uranium accumulation extracellularly and/or intracellularly to a varying degree. In Pseudomonas fluorescens and Bacillus subtilis uranium was associated with the cell surface and in the latter it was present as irregularly shaped grains. In Halobacterium halobium, the only archeon studied here, uranium was present as dense deposits and with Haloanaerobium praevalens as spikey deposits. Halomonas sp. isolated from the WIPP site accumulated uranium both extracellularly on the cell surface and intracellularly as electron-dense discrete granules. Extended X-ray absorption fine structure (EXAFS) analysis of uranium with the halophilic and non-halophilic bacteria and archaea showed that the uranium present in whole cells was bonded to an average of 2.4 ± 0.7 phosphoryl groups at a distance of 3.65 ± 0.03 Å. Comparison of whole cells of Halomonas sp. with the cell wall fragments of lysed cells showed the presence of a uranium bidentate complex at 2.91 ± 0.03 Å with the carboxylate group on the cell wall, and uranyl hydroxide with U−U interaction at 3.71 ± 0.03 Å due to adsorption or precipitation reactions; no U − P interaction was observed. Addition of uranium to the cell lysate of Halomonas sp. resulted in the precipitation of uranium due to the inorganic phosphate produced by the cells. These results show that the phosphates released from bacteria bind a significant amount of uranium. However, the bacterially immobilized uranium was readily solubilized by bicarbonate with concurrent release of phosphate into solution.

Complexation of Uranium by Cells and S-Layer Sheets of Bacillus sphaericus JG-A12

“…Extracellular association of uranium with bacterial cell surfaces is primarily due to physical and chemical interactions involving adsorption, ion exchange, and complexation and does not directly depend on metabolism. Bacterial cell walls, exopolymers, proteins, and lipids contain functional groups such as carboxylate, hydroxyl, amino, and phosphate, which are capable of forming complexes with uranium (19). A similar accumulation profile was found using another strain of B. sphaericus, strain JG-7B, isolated from the same uranium mining waste (39).…”

“…Most S-layers are 5 to 15 nm thick and possess pores of identical size and morphology in the range of 2 to 6 nm (6). As porous lattices completely covering the cell surface, the S-layers can provide prokaryotic cells with selective advantages by functioning as protective coats, as structures involved in cell adhesion and surface recognition, and as molecule or ion traps (53).Strong interest in sorption of U by bacterial surfaces as a method of U immobilization for the bioremediation of uranium-contaminated waters has resulted in numerous macroscopic, microscopic, and spectroscopic sorption studies of U by gram-positive and gram-negative bacteria (19,26,40,42). Microorganisms can mobilize radionuclides and metals through autotrophic and heterotrophic leaching, chelation by microbial metabolites and siderophores, and methylation, which can result in volatilization.…”

“…Strong interest in sorption of U by bacterial surfaces as a method of U immobilization for the bioremediation of uranium-contaminated waters has resulted in numerous macroscopic, microscopic, and spectroscopic sorption studies of U by gram-positive and gram-negative bacteria (19,26,40,42). Microorganisms can mobilize radionuclides and metals through autotrophic and heterotrophic leaching, chelation by microbial metabolites and siderophores, and methylation, which can result in volatilization.…”

The Confluence of Heavy Metal Biooxidation and Heavy Metal Resistance: Implications for Bioleaching by Extreme Thermoacidophiles

“…Further, in contrast to U(VI) biosorption in Chryseomonas sp. [276], Bacillus sphaericus ATCC 14577 [277], Pseudomonas fluorescence ATCC 55241 [271], and H. halobium [271] under corresponding experimental conditions, S. acidocaldarius has a significantly lower capability [269]. As noted above, bacteria have significantly different cell wall structures from archaea, which contain a large number of uranium binding ligands, such as carboxylic and phosphate groups [169,278].…”

“…The anaerobic hyperthermophile, Pyrobaculum islandicum, has been shown to reduce U(VI) to the insoluble U(IV) mineral uraninite leading to the formation of extracellular deposits [270]. Dense uranium deposits were observed at the cell surface in the halophilic archaeon Halobacterium halobium, with complexation of uranium predominantly via cellular inorganic phosphate (uranyl phosphate) [271]. More recently, the interaction of S. acidocaldarius with U(VI) was studied under highly acidic (pH 1.5-3.0) and moderately acidic (pH 4.5) conditions, relevant to the physiological growth optimum of this organism and uranium polluted environments [269,272].…”