Publication
Members of the Shewanella genus transfer electrons to metal and actinide electron acceptors such as hexavalent uranium, U(VI), via c-type cytochromes. The intracellular mechanism of electron transfer is well studied but the delivery of electrons to external electron acceptors less well so. MtrC, a decaheme c-type cytochrome located on the cell surface side of the outer membrane of many Shewanella species, and extending to the extracellular medium, transfers electrons to U(VI), both in vivo and in vitro when purified. However, it is unclear how the electron transfer between the terminal heme(s) of the protein and extracellular U(VI) occurs. In particular, the type of interaction between MtrC and U(VI), and the parameters controlling electron transfer remain to be elucidated. Here, we investigated the kinetics of U(VI) reduction by S. baltica MtrC in solution for U(VI) complexed with one of five ligands: carbonate, hydroxyl, citrate, nitrilotriacetic acid (NTA) or ethylenediaminetetraacetic acid (EDTA). We observed two initial reaction rates, one more rapid for U-citrate, U-NTA and U-EDTA, and another slower for U-carbonate and U-hydroxo. By combining Nuclear Magnetic Resonance spectroscopy and M 4-edge High Resolution X-ray Absorption Near Edge Structure spectroscopy, we attributed these differences to the type of interaction between the U-ligand complex and MtrC, i.e., probably electrostatic interaction with the ligand of U-EDTA, hydrogen bonding to the ligand of U-citrate and U-NTA, and covalent bonding with U-carbonate and U-hydroxo. We also demonstrate the persistence of U(V) in the U-carbonate system when interacting with MtrC. Overall, we showed that the mechanism of electron transfer depended on the chemistry of the soluble U(VI) complex serving as the substrate.