TY - JOUR
T1 - A 300-fold conductivity increase in microbial cytochrome nanowires due to temperature-induced restructuring of hydrogen bonding networks
AU - Dahl, Peter J.
AU - Yi, Sophia M.
AU - Gu, Yangqi
AU - Acharya, Atanu
AU - Shipps, Catharine
AU - Neu, Jens
AU - Patrick O’Brien, J.
AU - Morzan, Uriel N.
AU - Chaudhuri, Subhajyoti
AU - Guberman-Pfeffer, Matthew J.
AU - Vu, Dennis
AU - Yalcin, Sibel Ebru
AU - Batista, Victor S.
AU - Malvankar, Nikhil S.
N1 - Publisher Copyright:
Copyright © 2022 The Authors,
PY - 2022/5
Y1 - 2022/5
N2 - Although proteins are considered as nonconductors that transfer electrons only up to 1 to 2 nanometers via tunneling, Geobacter sulfurreducens transports respiratory electrons over micrometers, to insoluble acceptors or syntrophic partner cells, via nanowires composed of polymerized cytochrome OmcS. However, the mechanism enabling this long-range conduction is unclear. Here, we demonstrate that individual nanowires exhibit theoretically predicted hopping conductance, at rate (>1010 s−1) comparable to synthetic molecular wires, with negligible carrier loss over micrometers. Unexpectedly, nanowires show a 300-fold increase in their intrinsic conductance upon cooling, which vanishes upon deuteration. Computations show that cooling causes a massive rearrangement of hydrogen bonding networks in nanowires. Cooling makes hemes more planar, as revealed by Raman spectroscopy and simulations, and lowers their reduction potential. We find that the protein surrounding the hemes acts as a temperature-sensitive switch that controls charge transport by sensing environmental perturbations. Rational engineering of heme environments could enable systematic tuning of extracellular respiration.
AB - Although proteins are considered as nonconductors that transfer electrons only up to 1 to 2 nanometers via tunneling, Geobacter sulfurreducens transports respiratory electrons over micrometers, to insoluble acceptors or syntrophic partner cells, via nanowires composed of polymerized cytochrome OmcS. However, the mechanism enabling this long-range conduction is unclear. Here, we demonstrate that individual nanowires exhibit theoretically predicted hopping conductance, at rate (>1010 s−1) comparable to synthetic molecular wires, with negligible carrier loss over micrometers. Unexpectedly, nanowires show a 300-fold increase in their intrinsic conductance upon cooling, which vanishes upon deuteration. Computations show that cooling causes a massive rearrangement of hydrogen bonding networks in nanowires. Cooling makes hemes more planar, as revealed by Raman spectroscopy and simulations, and lowers their reduction potential. We find that the protein surrounding the hemes acts as a temperature-sensitive switch that controls charge transport by sensing environmental perturbations. Rational engineering of heme environments could enable systematic tuning of extracellular respiration.
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U2 - 10.1126/sciadv.abm7193
DO - 10.1126/sciadv.abm7193
M3 - Article
C2 - 35544567
AN - SCOPUS:85129956854
SN - 2375-2548
VL - 8
JO - Science Advances
JF - Science Advances
IS - 19
M1 - eabm7193
ER -