MgtE Homolog FicI Acts as a Secondary Ferrous Iron Importer in Shewanella oneidensis Strain MR-1.

The transport of metals into and out of cells is necessary for the maintenance of appropriate intracellular concentrations. Metals are needed for incorporation into metalloproteins but become toxic at higher concentrations. Many metal transport proteins have been discovered in bacteria, including the Mg2+ transporter E (MgtE) family of passive Mg2+/Co2+ cation-selective channels. Low sequence identity exists between members of the MgtE family, indicating that substrate specificity may differ among MgtE transporters. Under anoxic conditions, dissimilatory metal-reducing bacteria, such as Shewanella and Geobacter species, are exposed to high levels of soluble metals, including Fe2+ and Mn2+ Here we characterize SO_3966, which encodes an MgtE homolog in Shewanella oneidensis that we name FicI (ferrous iron and cobalt importer) based on its role in maintaining metal homeostasis. A SO_3966 deletion mutant exhibits enhanced growth over that of the wild type under conditions with high Fe2+ or Co2+ concentrations but exhibits wild-type Mg2+ transport and retention phenotypes. Conversely, deletion of feoB, which encodes an energy-dependent Fe2+ importer, causes a growth defect under conditions of low Fe2+ concentrations but not high Fe2+ concentrations. We propose that FicI represents a secondary, less energy-dependent mechanism for iron uptake by S. oneidensis under high Fe2+ concentrations.IMPORTANCEShewanella oneidensis MR-1 is a target of microbial engineering for potential uses in biotechnology and the bioremediation of heavy-metal-contaminated environments. A full understanding of the ways in which S. oneidensis interacts with metals, including the means by which it transports metal ions, is important for optimal genetic engineering of this and other organisms for biotechnology purposes such as biosorption. The MgtE family of metal importers has been described previously as Mg2+ and Co2+ transporters. This work broadens that designation with the discovery of an MgtE homolog in S. oneidensis that imports Fe2+ but not Mg2+ The research presented here also expands our knowledge of the means by which microorganisms have adapted to take up essential nutrients such as iron under various conditions.