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

Abstract

ABSTRACT 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 Mg 2+ transporter E (MgtE) family of passive Mg 2+ /Co 2+ 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 Fe 2+ and Mn 2+ . Here we characterize SO_3966, which encodes an MgtE homolog in Shewanella oneidensis that we name FicI ( f errous i ron and c obalt i mporter) 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 Fe 2+ or Co 2+ concentrations but exhibits wild-type Mg 2+ transport and retention phenotypes. Conversely, deletion of feoB , which encodes an energy-dependent Fe 2+ importer, causes a growth defect under conditions of low Fe 2+ concentrations but not high Fe 2+ concentrations. We propose that FicI represents a secondary, less energy-dependent mechanism for iron uptake by S. oneidensis under high Fe 2+ concentrations. IMPORTANCE Shewanella 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 Mg 2+ and Co 2+ transporters. This work broadens that designation with the discovery of an MgtE homolog in S. oneidensis that imports Fe 2+ but not Mg 2+ . 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.