Soil microbial community structure and functionality changes in response to long-term metal and radionuclide pollution.

Microbial communities are essential for a healthy soil ecosystem. Metals and radionuclides can exert a persistent pressure on the soil microbial community. However, little is known on the effect of long-term co-contamination of metals and radionuclides on the microbial community structure and functionality. We investigated the impact of historical discharges of the phosphate and nuclear industry on the microbial community in the Grote Nete river basin in Belgium. Eight locations were sampled along a transect to the river edge and one location further in the field. Chemical analysis demonstrated a metal and radionuclide contamination gradient and revealed a distinct clustering of the locations based on all metadata. Moreover, a relation between the chemical parameters and the bacterial community structure was demonstrated. Although no difference in biomass was observed between locations, cultivation-dependent experiments showed that communities from contaminated locations survived better on singular metals than communities from control locations. Furthermore, nitrification, a key soil ecosystem process seemed affected in contaminated locations when combining metadata with microbial profiling. These results indicate that long-term metal and radionuclide pollution impacts the microbial community structure and functionality and provides important fundamental insights into microbial community dynamics in co-metal-radionuclide contaminated sites.

PrsQ2, a small periplasmic protein involved in increased uranium resistance in the bacterium Cupriavidus metallidurans.

Uranium contamination is a widespread problem caused by natural and anthropogenic activities. Although microorganisms thrive in uranium-contaminated environments, little is known about the actual molecular mechanisms mediating uranium resistance. Here, we investigated the resistance mechanisms driving the adaptation of Cupriavidus metallidurans NA4 to toxic uranium concentrations. We selected a spontaneous mutant able to grow in the presence of 1 mM uranyl nitrate compared to 250 µM for the parental strain. The increased uranium resistance was acquired via the formation of periplasmic uranium-phosphate precipitates facilitated by the increased expression of a genus-specific small periplasmic protein, PrsQ2, regulated as non-cognate target of the CzcS2-CzcR2 two-component system. This study shows that bacteria can adapt to toxic uranium concentrations and explicates the complete genetic circuit behind the adaptation.

Molecular Mechanisms Underlying Bacterial Uranium Resistance.

Environmental uranium pollution due to industries producing naturally occurring radioactive material or nuclear accidents and releases is a global concern. Uranium is hazardous for ecosystems as well as for humans when accumulated through the food chain, through contaminated groundwater and potable water sources, or through inhalation. In particular, uranium pollution pressures microbial communities, which are essential for healthy ecosystems. In turn, microorganisms can influence the mobility and toxicity of uranium through processes like biosorption, bioreduction, biomineralization, and bioaccumulation. These processes were characterized by studying the interaction of different bacteria with uranium. However, most studies unraveling the underlying molecular mechanisms originate from the last decade. Molecular mechanisms help to understand how bacteria interact with radionuclides in the environment. Furthermore, knowledge on these underlying mechanisms could be exploited to improve bioremediation technologies. Here, we review the current knowledge on bacterial uranium resistance and how this could be used for bioremediation applications.

Cupriavidus metallidurans NA4 actively forms polyhydroxybutyrate-associated uranium-phosphate precipitates.

Cupriavidus metallidurans is a model bacterium to study molecular metal resistance mechanisms and its use for the bioremediation of several metals has been shown. However, its mechanisms for radionuclide resistance are unexplored. We investigated the interaction with uranium and associated cellular response to uranium for Cupriavidus metallidurans NA4. Strain NA4 actively captured 98 ± 1% of the uranium in its biomass after growing 24 h in the presence of 100 µM uranyl nitrate. TEM HAADF-EDX microscopy confirmed intracellular uranium-phosphate precipitates that were mainly associated with polyhydroxybutyrate. Furthermore, whole transcriptome sequencing indicated a complex transcriptional response with upregulation of genes encoding general stress-related proteins and several genes involved in metal resistance. More in particular, gene clusters known to be involved in copper and silver resistance were differentially expressed. This study provides further insights into bacterial interactions with and their response to uranium. Our results could be promising for uranium bioremediation purposes with the multi-metal resistant bacterium C. metallidurans NA4.