Metallic Conductivity in Proteins: A New Paradigm for Biological Electron Transfer and Bioelectronics
Electron transfer is central to all life processes. Every living cell must get rid of a large number of electrons left behind in metabolism when nutrients convert into energy. Aerobic organisms use oxygen to dump these electrons. Electron transfer in proteins occurs through either tunneling or hopping a few nanometers via inorganic cofactors. However, the common soil bacteria Geobacter sulfurreducens transfers electrons over hundreds of micrometers, to insoluble electron acceptors1 or syntrophic partner species2. Electron transfer is using hair-like protein filaments called pili1,2 that function as molecular nanowires and this allows bacteria to survive in environments that lack membrane-permeable electron acceptors such as oxygen. The conductivity of pili exhibits temperature dependence similar to that of disordered metallic polymers1,3. However, metallic conductivity is considered improbable in proteins due to the lack of periodicity in protein structure, thermal fluctuations, and low conductivity values.
I will present our recent electrical, optical and structural studies to identify the structural, molecular and physical mechanism of metallic conductivity in pili. 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, circular dichroism, fluorescence microscopy and infrared spectroscopy. Our studies suggest that aromatic amino acids in pili are closely packed from each other (< 4 Å), forming pi stacking, that can cause in intermolecular electron delocalization, conferring metallic conductivity to pili. Notably, we observe large conformational changes that accelerate electron transfer in pili. Furthermore, we show that improved metallic nature in the pili correlates with the improved pi stacking. These studies defy the current biochemical assumption that all proteins are electronic insulators and need inorganic cofactors for electron transfer. Pili thus represent a new class of electronically functional proteins that can transport electrons at rates and distances unprecedented in biology. I will discuss the implications of these studies for biological electron transfer as well as for bioelectronics.
 Malvankar et al. Nature Nanotechnology, 6, 573-579 (2011)
 Summers et al. Science, 330, 1413-1415 (2010)
 Malvankar et al. Nature Nanotechnology, 9, 1012-1017 (2014)