UNLABELLED: Most of Earth's iron is mineral-bound, but it is unclear how and to what extent iron-oxidizing microbes can use solid minerals as electron donors. A prime candidate for studying mineral-oxidizing growth and pathways is IMPORTANCE: Mineral-bound iron could be a vast source of energy to iron-oxidizing bacteria, but there is limited physiological evidence of this metabolism, and it has been unknown whether the mechanisms of solid and dissolved Fe(II) oxidation are distinct. In iron-reducing bacteria, multiheme cytochromes can facilitate iron mineral reduction, and here, we link a multiheme cytochrome-based pathway to mineral oxidation, expanding the known functionality of multiheme cytochromes. Given the growing recognition of microbial oxidation of minerals and cathodes, increasing our understanding of these mechanisms will allow us to recognize and trace the activities of mineral-oxidizing microbes. This work shows how solid iron minerals can promote microbial growth, which if widespread, could be a major agent of geologic weathering and mineral-fueled nutrient cycling in sediments, aquifers, and rock-hosted environments.