The Role of Spin in Extracellular Respiration of Metal-Reducing Bacteria

Electron transfer through chiral molecules, like biomolecules, is subject to the Chirality Induced Spin Selectivity (CISS) effect. This effect couples electron spin and velocity, potentially enhancing biological electron transport efficiency by suppressing backscattering. In metal-reducing bacteria, CISS might contribute to the rapid, long-distance extracellular electron transfer (EET) from the cellular interior to external solid-state minerals and electrodes facilitated by multiheme cytochromes. Previous studies confirmed spin selectivity in the surface multiheme cytochromes of the EET model organism Shewanella oneidensis MR-1. Here, we show that spin selectivity extends to the upstream membrane-associated decaheme MtrA and periplasmic tetraheme STC proteins using magnetic conductive atomic force microscopy (AFM). MtrA exhibits ~75% spin polarization, while STC shows ~35%. This suggests spin-dependent interactions throughout the entire extracellular respiration pathway.

We further demonstrate that the respiration of a biofilm of Geobacter sulfurreducens, another EET-capable bacterium, depends on the magnetization direction of the underlying electrode, aligning with the spin preference observed in conductive AFM measurements.

Taken collectively, our results demonstrate the important role of spin in biological electron transport mechanisms essential to life.