Multiple hops move electrons from bacteria to rocks.

The central dogma of bioenergetics is that photons energize electrons in molecules, those electrons push protons, and proton concentration gradients forge chemical bonds. An understanding of how this works—at the level of electrons and atoms—is elusive, especially in organisms that live life on the edge of survival. How do bacteria or bacterial cables move electrons between sources and sinks separated by micrometers to centimeters? In PNAS, van Wonderen et al. show that a heme-to-heme electron hopping transport mechanism enables the egress of electrons through the bacterial cell envelope in “rock-breathing” bacteria that use minerals as their terminal electron acceptors (1). The stunning discovery that some biological redox reactions can proceed at cryogenic temperatures (2) motivated the development of vibronically coupled electron-tunneling theories (3). Theory predicted that electron transfer (ET) reactions could occur over several nanometers on time scales as short as milliseconds, supporting the notion that electron tunneling could undergird molecular bioenergetics. Experimental studies of metal-labeled proteins (4, 5) and tunneling pathway theories (6) brought atomistic detail to the description of protein-mediated ET. These studies indicate that electron tunneling is enabled by both through-bond and through-space interactions, dictated by the molecular structure of the folded protein and by its cofactors. Electron transport through extracellular appendages (bacterial nanowires) on micrometer length scales is not reconciled by the theory of single-step electron tunneling (7). How can electrons exit the cell envelope and propagate for micrometers on biologically relevant timescales with little thermodynamic driving force? Modeling of nanowires requires that electron tunneling would have to occur between cofactors in near van der Waals (vdW) contact to explain the measured currents (7, 8). In PNAS, van Wonderen et al. report that transport in the decaheme MtrC protein, which enables electrons to flow across the bacterial cell envelope … [↵][1]1 Email: david.beratan{at}duke.edu. [1]: #xref-corresp-1-1