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

Abstract

Bacillus sphaericus JG-A12 is a natural isolate recovered from a uranium mining waste pile near the town of Johanngeorgenstadt in Saxony, Germany. The cells of this strain are enveloped by a highly ordered crystalline proteinaceous surface layer (S-layer) possessing an ability to bind uranium and other heavy metals. Purified and recrystallized S-layer proteins were shown to be phosphorylated by phosphoprotein-specific staining, inductive coupled plasma mass spectrometry analysis, and a colorimetric method. We used extended X-ray absorption fine-structure (EXAFS) spectroscopy to determine the structural parameters of the uranium complexes formed by purified and recrystallized S-layer sheets of B. sphaericus JG-A12. In addition, we investigated the complexation of uranium by the vegetative bacterial cells. The EXAFS analysis demonstrated that in all samples studied, the U(VI) is coordinated to carboxyl groups in a bidentate fashion with an average distance between the U atom and the C atom of 2.88 ؎ 0.02 Å and to phosphate groups in a monodentate fashion with an average distance between the U atom and the P atom of 3.62 ؎ 0.02 Å. Transmission electron microscopy showed that the uranium accumulated by the cells of this strain is located in dense deposits at the cell surface.Uranium is a long-lived radionuclide that is an ecological and human health hazard. The mining and processing of uranium for nuclear power plants and nuclear weapons production have resulted in the generation of significant amounts of radioactive wastes. The mobility of this radionuclide is controlled by its interaction with ions, minerals, and microorganisms present in nature. As a consequence of their small size and diverse metabolic activities, bacteria are able to interact intimately with metal ions present in their environment (15). Highly reactive bacterial cell surfaces bind uranium and other metal ions (7). This reactivity arises from the presence of a wide array of ionizable groups, such as carboxylate and phosphate, present in the lipopolysaccharides (LPS) of gram-negative bacterial cell walls (8) and the peptidoglycan, teichuronic acids, and teichoic acids of gram-positive bacteria (9).The bacterial cell wall may be overlayed by a number of surface structures, which can also interact with metal ions. These may be composed primarily of carbohydrate polymers (e.g., capsules) or proteinaceous surface layers (e.g., S-layers) and may occur singly or in combination (15). The crystalline bacterial cell S-layers represent the outermost cell envelope component of many bacteria and archaea (50). S-layers are generally composed of identical protein or glycoprotein subunits, and they completely cover the cell surface during all stages of bacterial growth and division. 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 s...

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