Mechanistic Understanding of Electronic Conductivity in Biological Structures via High Performance Computing

Multi-heme cytochromes (MHCs) have attracted much interest for use in nanobioelectronic junctions<br/>due to their high electronic conductances. Their charge transport mechanism has puzzled the community<br/>for many years, though experiment and computation now seem to have converged on a consistent picture.<br/><br/>An often overlooked aspect is that the transport mechanism in MHCs depends strongly on how the transport<br/>is induced: in the native biological environment electrons are injected in and ejected from the heme chain<br/>by molecular donors and acceptors that have a redox potential similar to the heme groups. Here, ultrafast<br/>pump-probe transient absorption spectroscopy and molecular simulation have shown that transport is<br/>via heme-to-heme electron hopping[1]. By contrast,in a junction the electron injection and ejection is facilitated<br/>by metallic electrodes with Fermi-levels that can differ substantially from the redox potentials of the heme groups,<br/>here by 1 eV [2]. Recent measurements on dry and aqueous MHC junctions as well as high performance<br/>computing suggested that a off-resonant coherent tunneling mechanism, not hopping, is operative over<br/>surprisingly long distances, up to about 7 nm [3]. We explain the long coherent tunneling distances by (i) a<br/>low exponential distance decay constant for coherent conduction (\beta = 0.2 Å−1), much lower than for biological<br/>electron transfer (\beta = 1.2-1.4 Å−1) (ii) a large density of protein electronic states that electronically couple<br/>to the electrodes, a factor of 10 higher than for typical molecular wires made of small molecules, prolonging the<br/>coherent tunneling regime to distances that exceed those in molecular wires [4].<br/><br/>In my talk I will consolidate this view by presenting new conductance calculations on MHC junctions where the<br/>number of hemes is systematically varied from 1 to 2 to 3 and 4 hemes and multiples of 4-heme protein<br/>chains approaching lengths of several 10 nanometers. I will also compare MHCs with cable bacteria which<br/>exhibit electronic conductances 3-4 orders of magnitudes higher than MHCs [5]. The transport scenario in cable<br/>bacteria is likely to be very different from the one in MHCs and potentially more similar to the one<br/>in highly conductive organic semiconductors or metal-organic frameworks.[6]<br/><br/>[1] J. H. van Wonderen, K. Adamczyk, X. Wu, X. Jiang, S. E. H. and Piper, C. R. Hall, M. J. Edwards, T. A. Clarke,<br/>H. Zhang, L. J. C. Jeuken, I. Sazanovich, M. Towrie, J. Blumberger, S. R. Meech, and J. N. Butt,<br/>“Nanosecond heme-to-heme electron transfer rates in a multiheme cytochrome nanowire reported by a spectrally<br/>unique His/Met ligated heme,” Proc. Nat. Acad. Sci. USA 118, e2107939118, 2021.<br/><br/>[2] Z. Futera, I. Ide, B. Kayser, K. Garg, X. Jiang, J. H. van Wonderen, J. N. Butt, H. Ishii, I. Pecht, M. Sheves, D. Cahen, and J. Blumberger,<br/>``Coherent electron transport across a 3 nm bioelectronic junction made of multi-heme proteins"<br/>J. Phys. Chem. Lett. 11, 9766-9774, 2020.<br/><br/>[3] Z. Futera, X. Wu, J. Blumberger, ``Tunneling-to-Hopping Transition in Multiheme Cytochrome Bioelectronic Junctions"<br/>J. Phys. Chem. Lett. 14, 445−452, 2023.<br/><br/>[4] Van Nguyen, Q.; Frisbie, C. D. Hopping Conductance in Molecular Wires Exhibits a Large Heavy-Atom KKinetic Isotope Effects.<br/>J. Am. Chem. Soc. 143, 2638−2643, 2021.<br/><br/>[5] Jasper R. van der Veen, Stephanie Valianti, Herre S. J. van der Zant, Yaroslav M. Blanter and Filip J. R. Meysman,<br/>``A model analysis of centimeter-long electron transport in cable bacteria" Phys. Chem. Chem. Phys. 26, 3139-3151, 2024.<br/><br/>[6] S. Giannini and J. Blumberger, “Charge transport in organic semiconductors: the perspective from non-adiabatic molecular dynamics,”<br/>Acc. Chem. Res., vol. 55, 819–830, 2022.