Interactions of U(VI) with archaea: what is different than with bacteria?

Archaea, in contrast to the diverse and dense bacterial populations, occur in uranium mining wastes in low numbers and belong mostly to particular crenarchaeal groups, some of them not yet cultured [1,2].
On the example of the termoacidophilic crenarchaeon Sulfolobus acidocaldarius, indigenous for many uranium contaminated wastes [3,4], we demonstrate that archaea tolerate substantially lower concentrations of U(VI) than bacteria and that they interact with this radionuclide in a significantly different way. One of the reasons for this behaviour is the unusual cell wall structure of the representatives of Crenarchaeota which is restricted to a single proteinaceous surface layer (S-layer), that is in contrary to the complex, rather thick, and rich on metal-binding ligands cell wall structure of bacteria. Due to the extreme acidic and mechanic stability of the S. acidocaldarius S-layer, it was possible to produce empty cells (ghosts) consisting only of the outermost S-layer membrane and to study their interactions with U(VI) at highly acidic (pH 1.5 and 3.0) and at moderate acidic (pH 4.5 and 6.0) conditions. Applying a set of modern spectroscopic techniques such as Time-Resolved Laser-induced Fluorescence (TRLF), X-ray Absorption, and Fourier-Transformed Infrared (FT-IR) we were able to clearly demonstrate that at highly acidic conditions the S. acidocaldarius S-layer does not play any protective role against the toxic U(VI). At these conditions low amounts of uranium are bound mainly by the phosphate groups of the cytoplasma membrane [5]. This finding is in distinction to the results obtained with S-layers of the bacterial isolates recovered from uranium mining wastes. The S-layers of the latter bind significant amounts of U(VI) and strongly contribute to the remarkable uranium resistance of their hosts [6]. The high capability of the mentioned bacterial S-layers to bind U(VI) was contributed to the fact that they are phosphorylated [6]. This feature is unusual for both bacterial and archaeal S-layers and is not the case for the S-layer of S. acidocaldarius [6, 7]. At moderate acidic conditions (pH 4.5), typical for most uranium mining wastes, the studied archaeal S-layer ghosts, again in contrast to the bacterial ones, bind insufficient amounts of U(VI) exclusively via the carboxylic groups of their carboxylated amino acid residues [7]. At pH 6.0, which is substantially above the growth optimum of S. acidocaldarius, the permeability of its cells is increased due to the pH stress and possibly also to the presence of U(VI). As a result uncontrolled uptake of U(VI) as well as release of phosphorylated biomolecules and also of orthophosphate occurs. These processes result initially in formation and precipitation of mixed uranyl phosphate phases. With the time the most part of U(VI) is bio-mineralized in inorganic mineral phases. The efficacy of these biomineralization processes is, however, much lower then those published for bacteria, possibly due to the lower amount of polyphosphatic granules in the studied archaeon [8].
We suggest that the limited presence of archaea in uranium wastes is related to their lower resistance to U(VI) which is determined by their cell wall structure and possibly also by some particular physiological and biochemical characteristics.

[1] Rastogi (2009) Microbial Ecology 58, 129-139. [2] Reitz (2007) FZR-Report 459, 42. [3] Marsh (1983] FEMS Microb. Lett., 17, 311-315. [4] Groudev (1993) FEMS Microb. Rev., 11, 260-268. [5] Reitz (2010) Radiochim Acta 98, 249-257. [6] Merroun (2005) Appl. Environ. Microbiol. 71, 5532-5543. [7] Reitz (2011] Radiochim Acta 99, 543-553. [8] Remonselez (2006) Microbiology, 152, 59-66.