Long-Range Electron Transfer across Cytochrome-Hematite (α-Fe2O3) Interfaces

Electrochemical scanning tunneling microscopy was used to assess the distance dependence of electron transfer facilitated by a bacterial multiheme cytochrome to a single crystal iron oxide surface. We measured tunneling current-distance (I-s) profiles across the nanoscale space between Au STM tips and the basal (001) surface of a hematite (alpha-Fe2O3) crystal and compared them to the case in which an intervening small tetraheme cytochrome (STC) from Shewanella oneidensis was covalently linked to the end of the Au tip. Tunneling profiles were collected at constant surface potentials in solutions having a range of ionic strengths. For the case without intervening cytochrome, at short tip-sample separation, the distance dependence of the tunneling current shows a quasi-linear behavior, whereas at longer distances, near-exponential decay is observed. The different regions can be understood first in terms of reduction of interfacial water and ion layers in the electrical double layer associated with the hematite surface, followed by electron tunneling through bulk water. The effective tunneling range and the transition between the two conduction mechanisms are substantially increased when STC is present in the tunneling junction, suggesting that cytochrome molecules provide enhanced tunneling pathways and stronger electronic coupling to the hematite surface. On the basis of these results, cytochrome-mediated electron transfer during bacterial metal reduction may be possible at distances farther than originally speculated. In addition, as multiheme cytochromes and other similar molecules gain attention for their promising role in fuel cells and molecular electronics, we demonstrate that the solution conditions and surface properties of the substrate must be carefully considered.