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Discovery and characterization of UipA, a uranium- and iron-binding PepSY protein involved in uranium tolerance by soil bacteria

A Correction to this article was published on 03 January 2022

This article has been updated

Abstract

Uranium is a naturally occurring radionuclide. Its redistribution, primarily due to human activities, can have adverse effects on human and non-human biota, which poses environmental concerns. The molecular mechanisms of uranium tolerance and the cellular response induced by uranium exposure in bacteria are not yet fully understood. Here, we carried out a comparative analysis of four actinobacterial strains isolated from metal and radionuclide-rich soils that display contrasted uranium tolerance phenotypes. Comparative proteogenomics showed that uranyl exposure affects 39–47% of the total proteins, with an impact on phosphate and iron metabolisms and membrane proteins. This approach highlighted a protein of unknown function, named UipA, that is specific to the uranium-tolerant strains and that had the highest positive fold-change upon uranium exposure. UipA is a single-pass transmembrane protein and its large C-terminal soluble domain displayed a specific, nanomolar binding affinity for UO22+ and Fe3+. ATR-FTIR and XAS-spectroscopy showed that mono and bidentate carboxylate groups of the protein coordinated both metals. The crystal structure of UipA, solved in its apo state and bound to uranium, revealed a tandem of PepSY domains in a swapped dimer, with a negatively charged face where uranium is bound through a set of conserved residues. This work reveals the importance of UipA and its PepSY domains in metal binding and radionuclide tolerance.

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Fig. 1: Interactions of Microbacterium strains ViU2A, HG3, A9 and ViU22 with uranium.
Fig. 2: Characterization of uranyl coordination by FTIR and EXAFS spectroscopy.
Fig. 3: Crystallographic structure of UipAext-ViU2A.
Fig. 4: Working model showing the genomic organization of uipRS and A genes, and the proposed mechanism of U sensing and the function of UipA.

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Acknowledgements

This work was supported by the Toxicology program of the CEA (BEnUr project), the CNRS/CEA/AREVA NEEDS-Ressources Program (SURE project) and the CNRS/IRSN GDR TRASSE program. The PhD grants of Nicolas Gallois and Abbas Mohamad Ali were funded by the PhD program of the CEA. The PhD grant of Nicolas Theodorakopoulos was funded by the IRSN/PACA regional council. We thank the AFMB lab (Marseille, France) for the use of the rotating anode. This work has benefitted from the facilities and expertize of the PROXIMA-1 beam line for XRD and MARS beam line for EXAFS at the SOLEIL synchrotron, Saint Aubin, France. We warmly thank Séverine Zirah for providing us with the HG3 strain used in this study, and Badreddine Douzi for the pKtop plasmid.

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VC designed and supervised the study. VC and LP performed the uranium exposure experiments and prepared the samples for proteomics. NT, MF and LF performed microscopic analysis and ICP-AES measurements. BAB acquired the proteomics data and NG, BA-B and JA performed the proteomic analyses. PO and MB performed genomic and phylogenetic analyses and constructed ORF databases for proteomics. AMA established UipA topology in vivo. NG purified the recombinant proteins and performed fluorescence titration experiments, assisted by NB, NG and DL performed native mass spectrometry experiments. NG acquired FTIR data under CB supervision. NG prepared the samples for synchrotron-based analysis and participated in EXAFS data acquisition. CDA performed EXAFS data acquisition and processing. NB and NG performed crystallization tests and obtained the protein crystals under supervision of PA. PA and PL resolved the UipA structure. NG, BA-B, PO, MB, NB, AMA, DL, CDA, PA, CB, JA and VC analyzed the data. NG and VC wrote the paper and PO, MB, LF, DL, CDA, PA, CB. BA-B and JA edited it.

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Correspondence to Virginie Chapon.

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Gallois, N., Alpha-Bazin, B., Bremond, N. et al. Discovery and characterization of UipA, a uranium- and iron-binding PepSY protein involved in uranium tolerance by soil bacteria. ISME J 16, 705–716 (2022). https://doi.org/10.1038/s41396-021-01113-7

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