Abstract Electron Spin as a Functional Parameter in Biological Electron Transfer Nir Sukenik 1 , Sukrampal Yadav 1 , Cole C. Harris 1 , Marko Chavez 2 , Lech T. Baczewski 3 , and Mohamad Y. El-Naggar 1
1. Department of Physics and Astronomy, University of Southern California, Los Angeles, CA, United States 2. Omenn-Darling Bioengineering Institute, Princeton University, Princeton, NJ, United States 3. Institute of Physics, Polish Academy of Sciences, Warsaw, Poland
Keywords: Chirality-induced spin selectivity (CISS), Extracellular electron transfer (EET), Multiheme cytochromes, Biological electron transfer
Biological energy conversion requires highly efficient electron transfer (ET) to sustain metabolism and prevent the generation of destructive chemical byproducts. While ET in cells typically occurs through chiral protein structures composed of intrinsically non-conductive organic materials, it proceeds with remarkable fidelity, facilitating efficient, directional transport along specific biomolecular pathways. The Chiral Induced Spin Selectivity (CISS) effect, which couples electron spin to linear momentum during transport through chiral media 1 , offers a compelling mechanism underlying this efficiency. This spin-momentum coupling is proposed to enhance ET efficiency by suppressing backscattering, thereby promoting directional charge flow 2,3 .
While spin-selective electron transport has been previously demonstrated in isolated chiral biomolecules under dry, non-physiological conditions 4–6 , its in vivo significance remains unknown. Extracellular electron transfer (EET) by certain anaerobic bacteria provides a unique and tractable handle to test the functional relevance of CISS under physiological conditions. During EET, electrons derived from intracellular metabolism are transported through a network of multiheme cytochromes across the cellular membrane to extracellular insoluble electron acceptors. This extracellular respiration process can be directly monitored electrochemically via current production.
Here, we demonstrate spin-dependent electron transport through the active EET pathway of living Geobacter sulfurreducens bacterial biofilms cultivated on a working electrode. By monitoring respiratory current production during growth on oppositely magnetized substrates and upon in situ magnetization reversal of a ferromagnetic electrode, we observe a consistent preference for a specific spin orientation that matches previous reports for isolated cytochromes. These results provide direct in vivo evidence that spin selectivity persists under physiological conditions, establishing electron spin as a fundamental operative parameter in biological electron transfer, and open new questions about the importance of the electron spin in a wide range of biological systems.
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