DOI: 10.1021/jacs.6c11008 ISSN: 0002-7863

Heme-Mediated Charge Transport Modulation: Coupling Biological Recognition to Solid-State Protein Electronics

Kethavath Hemanth Naik, Aswin Sivankutty, Bony Johns Mathew, Joel George Reji, Ansalna Kalarickal Rasheed, Divyajyothi Kadamkot, Rinsha Cholasseri, Puthan Veetil Muhasina, Susmita De, Jerry Alfred Fereiro

Abstract

Integrating the selectivity of biological recognition with the robustness of solid-state electronics remains a formidable challenge. Here, we demonstrate the functional integration of myoglobin (Mb) and its heme-depleted analogue, apomyoglobin (apoMb), within lithographically defined gold (Au) nanogap junctions bridged by Au nanowires (AuNWs). Electronic measurements reveal that the heme cofactor facilitates electron transport (ETp), with oxygen (O2) coordination at the Fe center modulating ETp by up to ∼ 10-fold. In contrast, apoMb junctions lacking the heme cofactor exhibit uniformly low conductance with negligible O2 sensitivity. QM/MM and EDA-NOCV analyses indicate that O2 coordination induces a charge-separated Fe3+–O2– configuration, characterized by combined Fe3+←O2̅ donor–acceptor π and Fe3+↔O2̅ σ-bonding interactions. This charge polarization toward O2 redistributes electron density away from the Fe center, resulting in strong π-back-donation, which destabilizes the Fe-centered antibonding orbitals, shifting the LUMO of MbO2 (Fe–O2 π*) to a higher energy consistent with the observed increase in tunneling barrier. Ultraviolet photoelectron spectroscopy (UPS) further reveals distinct HOMOonset values for Mb and apoMb monolayers, directly linking cofactor presence to electronic coupling. Collectively, our findings establish a clear mechanistic link between heme-mediated gas recognition coupled to ETp, providing a framework for integrating biological recognition with solid-state electronic devices within a single platform.