Invited Talk 21st International Conference on Biological Inorganic Chemistry 2025

Electron transfer and electronic conductance in multi-heme cytochromes (121561)

Jochen Blumberger 1 , Andras Petho 1
  1. University College London (UCL), LONDON, United Kingdom

Multi-heme cytochromes (MHCs) have attracted much interest for use in nanobioelectronic junctions
due to their high electronic conductances. Their charge transport mechanism has puzzled the community
for many years, though experiment and computation now seem to have converged on a consistent picture.
An often overlooked aspect is that the transport mechanism in MHCs depends strongly on how the transport
is induced: in the native biological environment electrons are
injected in and ejected from the heme chain by molecular donors and acceptors that have a
redox potential similar to the heme groups. Here, ultrafast pump-probe transient absorption spectroscopy
and molecular simulation have shown that transport is via heme-to-heme electron hopping[1]. By contrast,
in a junction the electron injection and ejection is facilitated by metallic electrodes with Fermi-levels
that can differ substantially from the redox potentials of the heme groups, here by 1 eV [2]. Recent
measurements on dry and aqueous MHC junctions as well as high performance computing suggested that a
off-resonant coherent tunneling mechanism, not hopping, is operative over surprisingly long distances,
up to about 7 nm [3]. We explain the long coherent tunneling distances by (i) a low exponential distance decay constant for coherent conduction
(\beta = 0.2 Å−1), much lower than for biological electron transfer (\beta = 1.2-1.4 Å−1)
(ii) a large density of protein electronic states that electronically couple to the electrodes, a factor
of 10 higher than for typical molecular wires made of small molecules, prolonging the coherent tunneling
regime to distances that exceed those in molecular wires [4]. In my talk
I will consolidate this view by presenting new conductance calculations on MHC junctions where the
number of hemes is systematically varied from 1 to 2, 3, 4, 5 and 6 hemes and multiples of 4-heme protein
chains approaching lengths of several 10 nanometers.[5] I will also compare MHCs with cable bacteria which
exhibit electronic conductances 3-4 orders of magnitudes higher than MHCs [6]. The transport scenario in cable
bacteria is likely to be very different from the one in MHCs and potentially more similar to the one
in highly conductive organic semiconductors or metal-organic frameworks. [7]

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  2. [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, ``Coherent electron transport across a 3 nm bioelectronic junction made of multi-heme proteins" J. Phys. Chem. Lett. 11, 9766-9774, 2020.
  3. [3] Z. Futera, X. Wu, J. Blumberger, ``Tunneling-to-Hopping Transition in Multiheme Cytochrome Bioelectronic Junctions" J. Phys. Chem. Lett. 14, 445−452, 2023.
  4. [4] Van Nguyen, Q.; Frisbie, C. D. Hopping Conductance in Molecular Wires Exhibits a Large Heavy-Atom KKinetic Isotope Effects. J. Am. Chem. Soc. 143, 2638−2643, 2021.
  5. [5] A. Petho, Z. Futera, J. Blumberger, manuscript in preparation.
  6. [6] Jasper R. van der Veen, Stephanie Valianti, Herre S. J. van der Zant, Yaroslav M. Blanter and Filip J. R. Meysman, ``A model analysis of centimeter-long electron transport in cable bacteria" Phys. Chem. Chem. Phys. 26, 3139-3151, 2024.
  7. [7] S. Giannini and J. Blumberger, “Charge transport in organic semiconductors: the perspective from non-adiabatic molecular dynamics,” Acc. Chem. Res., vol. 55, 819–830, 2022.