ABSTRACTA novel halophilic and metal-reducing bacterium,Orenia metallireducensstrain Z6, was isolated from briny groundwater extracted from a 2.02 km-deep borehole in the Illinois Basin, IL. This organism shared 96% 16S rRNA gene similarity withOrenia marismortuibut demonstrated physiological properties previously unknown for this genus. In addition to exhibiting a fermentative metabolism typical of the genusOrenia, strain Z6 reduces various metal oxides [Fe(III), Mn(IV), Co(III), and Cr(VI)], using H₂as the electron donor. Strain Z6 actively reduced ferrihydrite over broad ranges of pH (6 to 9.6), salinity (0.4 to 3.5 M NaCl), and temperature (20 to 60°C). At pH 6.5, strain Z6 also reduced more crystalline iron oxides, such as lepidocrocite (γ-FeOOH), goethite (α-FeOOH), and hematite (α-Fe₂O₃). Analysis of X-ray absorption fine structure (XAFS) following Fe(III) reduction by strain Z6 revealed spectra from ferrous secondary mineral phases consistent with the precipitation of vivianite [Fe₃(PO₄)₂] and siderite (FeCO₃). The draft genome assembled for strain Z6 is 3.47 Mb in size and contains 3,269 protein-coding genes. Unlike the well-understood iron-reducingShewanellaandGeobacterspecies, this organism lacks thec-type cytochromes for typical Fe(III) reduction. Strain Z6 represents the first bacterial species in the genusOrenia(orderHalanaerobiales) reported to reduce ferric iron minerals and other metal oxides. This microbe expands both the phylogenetic and physiological scopes of iron-reducing microorganisms known to inhabit the deep subsurface and suggests new mechanisms for microbial iron reduction. These distinctions from otherOreniaspp. support the designation of strain Z6 as a new species,Orenia metallireducenssp. nov.IMPORTANCEA novel iron-reducing species,Orenia metallireducenssp. nov., strain Z6, was isolated from groundwater collected from a geological formation located 2.02 km below land surface in the Illinois Basin, USA. Phylogenetic, physiologic, and genomic analyses of strain Z6 found it to have unique properties for iron reducers, including (i) active microbial iron-reducing capacity under broad ranges of temperatures (20 to 60°C), pHs (6 to 9.6), and salinities (0.4 to 3.5 M NaCl), (ii) lack ofc-type cytochromes typically affiliated with iron reduction inGeobacterandShewanellaspecies, and (iii) being the only member of theHalanaerobialescapable of reducing crystalline goethite and hematite. This study expands the scope of phylogenetic affiliations, metabolic capacities, and catalytic mechanisms for iron-reducing microbes.