Uranium-tolerant soil bacteria protect Arabidopsis thaliana seedling growth from uranium toxicity

Uranium (U) is a naturally occurring radioelement that is chemically toxic to all living organisms. We investigated the effect of U on Arabidopsis thaliana seed germination and the early stages of seedling development. We showed that U had very little effect on Arabidopsis seed germination, with germination rates above 90% at 500 µM uranyl nitrate. However, U had a drastic effect on the Arabidopsis seedling development and the root was the most U-sensitive organ, with severe growth inhibition (>75%) starting at 20 µM uranyl nitrate. We showed that the two soil bacterial strains Microbacterium sp. ViU2A and Stenotrophomonas bentonitica BII-R7, which are able to tolerate high concentrations of U, strongly reduced the toxic effects of U on seedling development. Thus, in the presence of both strains, root growth inhibition was prevented up to 100 µM uranyl nitrate. This protection was specific to U-tolerant soil bacteria, as Escherichia coli was unable to protect seedlings. The analysis of U distribution between Arabidopsis seedlings and soil bacteria showed that the protective effect of bacteria was due to their ability to sequester U, either by biosorption at the cell surface and/or by intracellular or extracellular biomineralization. Also, the ability of both soil bacterial strains to prevent U toxicity was much less efficient when dead bacteria were used, suggesting the involvement of metabolism-dependent biological processes in seedling protection. Accordingly, we showed that the Uranium-induced protein A (UipA) contributes to the protection of Arabidopsis seedlings by Microbacterium sp. ViU2A. This study suggests that U-tolerant soil bacteria may be useful for phytostabilization strategies of U-contaminated soils and for limiting the entry of this toxic element into crops.