Mechanism of metal-like transport in bacterial protein nanowires

Who: Dr. Nikhil Malvankar & Sibel Yalcin, Yale University
Thursday, September 20, 2018 - 4:00pm
321 Allen Hall

A cornerstone of quantum physics is the interference of electron waves arising from the superposition principle. Metallic conductivity is an effect of interference of partial electron waves multiply scattered at the ion cores of the crystal lattice. But proteins are generally insulators. Electron transfer in proteins occurs through either tunneling or hopping a few nanometers via inorganic cofactors. However, the common soil bacteriaGeobacter sulfurreducens transfer electrons over hundreds of micrometers, to insoluble electron acceptors1 or syntrophic partner species2 for respiration and sharing of energy. These bacteria use helical protein filaments on their surface for extracellular electron transport, allowing them to survive in environments that lack membrane-permeable electron acceptors such as oxygen1,2. Near room temperature, the conductivity of wild-type filaments exhibits temperature dependence similar to that of metallic polymers1,3 which recently was confirmed independently4. However, the mechanism of conductivity has remained unclear.

I will present our recent structural, molecular and biophysical studies to identify the mechanism of metallic-like conductivity in filaments. We elucidate the physical mechanism of electron transport by measuring the electrical and optical conductivity of filaments from multiple mutant strains as a function of molecular length, temperature, frequency, pH and aromatic stacking. We demonstrate that intrinsic conductivity of individual filaments can be accurately described by nearest-neighbor, tight-binding model as predicted theoretically for quasi-one-dimensional materials. To determine the molecular architecture responsible for conductivity, we are using a suite of complementary experimental and computational methods such as molecular dynamics, x-ray diffraction and near-atomic resolution cryo-electron microscopy. Our studies suggest that filaments show π-stacking, that can cause intermolecular electron delocalization, conferring metallic conductivity to filaments. Furthermore, increasing π-stacking improves their crystallinity, yielding a longer mean free path for electrons, and stronger electronic coupling which yields 1000 times lower electron attenuation than other proteins. These protein nanowires thus represent a new class of functional biomaterials that can transport electrons at rates and distances unprecedented in biology. These findings will help development of genetically programmable biomolecular materials with tunable functionality through precise control of their electronic and protein structure.

[1] Malvankar et al. Nature Nanotechnology, 6, 573-579 (2011)

[2] Summers et al. Science, 330, 1413-1415 (2010)

[3] Malvankar et al. Nature Nanotechnology, 9, 1012-1017 (2014)

[4] Ing et al. Phys. Chem. Chem. Phys. 19, 21791 (2017)