Multistage bioassociation of uranium onto an extremely halophilic archaeon revealed by a unique combination of spectroscopic and microscopic techniques

Abstract

The interactions of two extremely halophilic archaea with uranium were investigated at high ionic strength as a function of time, pH and uranium concentration. Halobacterium noricense DSM-15987 and Halobacterium sp. putatively noricense, isolated from the Waste Isolation Pilot Plant repository, were used for these investigations. The kinetics of U(VI) bioassociation with both strains showed an atypical multistage behavior, meaning that after an initial phase of U(VI) sorption, an unexpected interim period of U(VI) release was observed, followed by a slow reassociation of uranium with the cells. By applying in situ attenuated total reflection Fourier-transform infrared spectroscopy, the involvement of phosphoryl and carboxylate groups in U(VI) complexation during the first biosorption phase was shown. Differences in cell morphology and uranium localization become visible at different stages of the bioassociation process, as shown with scanning electron microscopy in combination with energy dispersive X-ray spectroscopy. Our results demonstrate for the first time that association of uranium with the extremely halophilic archaeon is a multistage process, beginning with sorption and followed by another process, probably biomineralization.

How to Cope With Heavy Metal Ions: Cellular and Proteome-Level Stress Response to Divalent Copper and Nickel in Halobacterium salinarum R1 Planktonic and Biofilm Cells

“…One mechanism is the active copper export via the P 1 -type Cu(II)-efflux ATPase YvgX as demonstrated in H. salinarum NCR-1 (Kaur et al, 2006). Moreover, uranium association to haloarchaeal cell surfaces was reported (Bader et al, 2017) as well as copper ion binding and storage, which is presumably mediated by copper-binding metallochaperones (Pang et al, 2013). Enzymatic detoxification, i.e., reduction or modification of the metal ions, such as methylation, were both proposed to contribute to arsenic resistance (Wang et al, 2004).…”

Comparative analysis of uranium bioassociation with halophilic bacteria and archaea

“…noricense DSM15987 T was purchased from the Leibniz Institute DSMZ - German Collection of Microorganisms and Cell Cultures (DSMZ, Braunschweig, Germany). It was cultivated in modified DSM372 medium [ 11 ]. During growth, the cultures were shaken at 140 rpm in the dark in a water bath at 30°C.…”

“…After washing, a defined amount of H . noricense cells was pelleted and resuspended in 10 mL uranium solution, pC H+ 6, containing 3 M NaCl [ 11 ]. After exposure, the suspension was centrifuged (18°C, 10,000 x g , 10 min).…”

“…Nevertheless, it is important to include thermodynamics and interaction mechanisms of all possible microorganisms in the safety assessment of a potential repository. Only a few studies have been reported regarding the investigation of halophilic microorganisms with radionuclides [ 11 – 14 ]. A study by Francis and coworkers [ 12 ] compared the interactions of halophilic archaea and bacteria, as well as non-halophilic bacteria, with uranium.…”

Diversity and Niche of Archaea in Bioremediation

“…The archaeon Halobacterium noricense DSM15987 was found to accumulate U IV with phosphoryl and carboxylate groups compared to a direct biosorption process with the bacterium Brachybacterium sp. G1 [ 127 , 128 ]. These results show promise that the haloarchaea can be used in the treatment of hypersaline environments and wastewaters for heavy metal removals.…”