Electron Spin Effects in Extracellular Electron Transport Proteins

Electron transfer through chiral molecules is characterized by a coupling between the electron velocity and its spin through the Chirality Induced Spin Selectivity (CISS) effect. Since most biomolecules are homochiral, it was recently hypothesized that CISS underlies the highly efficient electron transfer observed in biological systems by reducing the probability of electron backscattering. A remarkable example of fast, efficient, and long-distance electron transport in biology is the extracellular respiration of metal-reducing bacteria, where a pathway composed of multiheme cytochromes facilitates extracellular electron transfer (EET) from the cellular interior to external solid-state minerals and electrodes. Previous studies of the cell surface multiheme cytochromes from the EET model organism <i>Shewanella oneidensis</i> MR-1 confirmed their spin selective transport properties. Using conductive probe atomic force microscopy (AFM) measurements of protein monolayers adsorbed onto ferromagnetic substrates, we show that electron transport is also spin selective in two of the upstream cellular multiheme `wire proteins’ – the membrane-associated decaheme MtrA and the tetraheme periplasmic STC. Moreover, we have determined the spin polarization of MtrA to be <b>~75% </b>and STC to be ~35%. These results suggest that spin-dependent interactions affect the entire extracellular respiration pathway.<br/>To assess the <i>in vivo</i> physiological impact of CISS, we also present compelling evidence that the respiration of <i>Geobacter sulfurreducens</i>, an EET-capable bacterium that forms thick electrochemically active biofilms, depends on the magnetization direction of the underlying ferromagnetic electrode. Electron exchange between <i>G. sulfurreducens </i>and the working electrode is enhanced in the same magnetization direction as the spin preference revealed from conductive AFM measurements. Taken collectively, our results demonstrate the important role of spin in biological electron transport mechanisms essential to life.