A riboswitch-controlled manganese exporter (Alx) tunes intracellular Mn2+concentration inE. coliat alkaline pH
bioRxiv (Cold Spring Harbor Laboratory)(2023)
Abstract
Abstract Cells use transition metal ions as structural components of biomolecules and cofactors in enzymatic reactions, making transition metals vital cellular components. The buildup of a particular metal ion in certain stress conditions becomes harmful to the organism due to the misincorporation of the excess ion into biomolecules, resulting in perturbed enzymatic activity or metal-catalyzed formation of reactive oxygen species. Organisms optimize metal concentration by regulating the expression of proteins that import and export that metal, often in a metal concentration-dependent manner. One such regulation mechanism is via riboswitches, which are 5’-untranslated regions (UTR) of an mRNA that undergo conformational changes to promote or inhibit the expression of the downstream gene, commonly in response to a ligand. The yybP-ykoY family of bacterial riboswitches shares a conserved aptamer domain that binds manganese (Mn 2+ ). In E. coli , the yybP-ykoY riboswitch precedes and regulates the expression of two genes: mntP , which based on extensive genetic evidence encodes an Mn 2+ exporter, and alx , which encodes a putative metal ion transporter whose cognate ligand is currently in question. Expression of alx is upregulated by both elevated intracellular concentrations of Mn 2+ and alkaline pH. With metal ion measurements and gene expression studies, we demonstrate that the alkalinization of media increases cytoplasmic Mn 2+ content, which in turn enhances alx expression. Alx then exports excess Mn 2+ to prevent toxic buildup of the metal inside the cell, with the export activity maximal at alkaline pH. Using mutational and complementation experiments, we pinpoint a set of acidic residues in the predicted transmembrane segments of Alx that play a crucial role in its Mn 2+ export. We propose that Alx-mediated Mn 2+ export provides a primary protective layer that fine-tunes the cytoplasmic Mn 2+ levels, especially during alkaline stress.
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Key words
manganese exporter,intracellular mn<sup>2+</sup>concentration,alkaline,riboswitch-controlled
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