Long distance electron transfer through the aqueous solution between redox partner proteins

Anna Lagunas,Pau Gorostiza,Alejandra Guerra-Castellano,Miguel A De La Rosa,Carme Rovira,Josep Samitier,Alba Nin-Hill,Irene Díaz-Moreno

doi:10.1038/s41467-018-07499-x

Abstract

Despite the importance of electron transfer between redox proteins in photosynthesis and respiration, the inter-protein electron transfer rate between redox partner proteins has never been measured as a function of their separation in aqueous solution. Here, we use electrochemical tunneling spectroscopy to show that the current between two protein partners decays along more than 10 nm in the solution. Molecular dynamics simulations reveal a reduced ionic density and extended electric field in the volume confined between the proteins. The distance-decay factor and the calculated local barrier for electron transfer are regulated by the electrochemical potential applied to the proteins. Redox partners could use electrochemically gated, long distance electron transfer through the solution in order to conciliate high specificity with weak binding, thus keeping high turnover rates in the crowded environment of cells.

Highlights

Despite the importance of electron transfer between redox proteins in photosynthesis and respiration, the inter-protein electron transfer rate between redox partner proteins has never been measured as a function of their separation in aqueous solution
Cc forms a natural complex with the cytochrome c1 (Cc1) subunit of cytochrome bc[1]
Human Cc1 has not yet been obtained in soluble form, this interaction can be conveniently studied within the well-characterized cross complex between human cytochrome c and the soluble domain of plant cytochrome Cc113, which were respectively bound to the electrochemical tunneling spectroscopy (ECTS) probe and sample electrodes

Summary

Introduction

Despite the importance of electron transfer between redox proteins in photosynthesis and respiration, the inter-protein electron transfer rate between redox partner proteins has never been measured as a function of their separation in aqueous solution. The demands on the electron transfer (ET) capabilities of these proteins are conflicting: their binding must be tight in order to keep ET rates high, but binding should be sufficiently weak to allow a high turnover rate and overall ET efficiency These demands can be traded off by a stepwise association process between the protein partners: as the distance between redox partners is reduced, an initial encounter complex is formed that leads to a final active complex in which ET occurs between the redox-active sites located within nanometer-scale proximity[3]. The distance-dependence of interprotein ET has been studied in various protein partners and mutants that alter the geometry of the wild-type complex, which leads to different distances between active sites, and coupling mechanisms[5]. The distance decay factor is regulated by the electrochemical potential applied to the proteins, which highlights the physiological relevance of these results

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