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

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journal contribution
posted on 14.08.2017, 00:00 by Tatsuya Fukushima, Sayan Gupta, Behzad Rad, Jose A. Cornejo, Christopher J. Petzold, Leanne Jade G. Chan, Rena A. Mizrahi, Corie Y. Ralston, Caroline M. Ajo-Franklin
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.