The Molecular Basis for Binding of an Electron Transfer Protein to a Metal Oxide Surface

Journal of the American Chemical Society

5 years ago

The Molecular Basis for Binding of an Electron Transfer Protein to a Metal Oxide Surface

Sayan Gupta, Behzad Rad, Caroline M. Ajo-Franklin, Rena A. Mizrahi, Christopher J. Petzold, Corie Y. Ralston, Jose A. Cornejo, Tatsuya Fukushima, Leanne Jade G. Chan

Achieving fast electron transfer between a material and protein is a long-standing challenge confronting applications in bioelectronics, bioelectrocatalysis, and optobioelectronics. Interestingly, naturally occurring extracellular electron transfer proteins bind to and reduce metal oxides fast enough to enable cell growth, and thus could offer insight into solving this coupling problem. While structures of several extracellular electron transfer proteins are known, an understanding of how these proteins bind to their metal oxide substrates has remained elusive because this abiotic–biotic interface is inaccessible to traditional structural methods. Here, we use advanced footprinting techniques to investigate binding between the Shewanella oneidensis MR-1 extracellular electron transfer protein MtrF and one of its substrates, α-Fe₂O₃ nanoparticles, at the molecular level. We find that MtrF binds α-Fe₂O₃ specifically, but not tightly. Nanoparticle binding does not induce significant conformational changes in MtrF, but instead protects specific residues on the face of MtrF likely to be involved in electron transfer. Surprisingly, these residues are separated in primary sequence, but cluster into a small 3D putative binding site. This binding site is located near a local pocket of positive charge that is complementary to the negatively charged α-Fe₂O₃ surface, and mutational analysis indicates that electrostatic interactions in this 3D pocket modulate MtrF–nanoparticle binding. Strikingly, these results show that binding of MtrF to α-Fe₂O₃ follows a strategy to connect proteins to materials that resembles the binding between donor–acceptor electron transfer proteins. Thus, by developing a new methodology to probe protein–nanoparticle binding at the molecular level, this work reveals one of nature’s strategies for achieving fast, efficient electron transfer between proteins and materials.

Publisher URL: http://dx.doi.org/10.1021/jacs.7b06560

DOI: 10.1021/jacs.7b06560