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Title: Possible Dynamically Gated Conductance along Heme Wires in Bacterial Multiheme Cytochromes

Abstract

The staggered cross decaheme configuration of electron transfer co-factors in the outer-membrane cytochrome MtrF may serve as a prototype for conformationally-gated multi-heme electron transport. Derived from the bacterium Shewanella oneidensis, the staggered cross configuration reveals intersecting c-type octaheme and tetraheme “wires” containing thermodynamic “hills” and “valleys”, suggesting that the protein structure may include a dynamical mechanism for conductance and pathway switching depending on enzymatic functional need. Recent molecular simulations have established the pair-wise electronic couplings, redox potentials, and reorganization energies to predict the maximum conductance along the various heme wire pathways by sequential hopping of a single electron (PNAS (2014) 11,611-616). Here, we expand this information with classical molecular and statistical mechanics calculations of large-amplitude protein dynamics in MtrF, to address its potential to modulate pathway conductance, including assessment of the effect of the total charge state. Explicit solvent molecular dynamics simulations of fully oxidized and fully reduced MtrF employing ten independent 50-ns simulations at 300 K and 1 atm showed that reduced MtrF is more expanded and explores more conformational space than oxidized MtrF, and that heme reduction leads to increased heme solvent exposure. The slowest mode of collective decaheme motion is 90% similar between the oxidized and reducedmore » states, and consists primarily of inter-heme separation with minor rotational contributions. The frequency of this motion is 1.7×107 s 1 for fully-oxidized and fully-reduced MtrF, respectively, slower than the downhill electron transfer rates between stacked heme pairs at the octaheme termini and faster than the electron transfer rates between parallel hemes in the tetraheme chain. This implies that MtrF uses slow conformational fluctuations to modulate electron flow along the octaheme pathway, apparently for the purpose of increasing the residence time of electrons on lowest potential hemes 4 and 9. This apparent gating mechanism should increase the success rate of electron transfer from MtrF to low potential environmental acceptors via these two solvent-exposed hemes.« less

Authors:
;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1172458
Report Number(s):
PNNL-SA-101673
48205; KP1702030
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Journal of Physical Chemistry B, 118(29):8505–8512
Additional Journal Information:
Journal Name: Journal of Physical Chemistry B, 118(29):8505–8512
Country of Publication:
United States
Language:
English
Subject:
c-type cytochromes, MtrF, Shewanella oneidensis, hemes (haems), molecular dynamics, conformationally-gated electron transport; Environmental Molecular Sciences Laboratory

Citation Formats

Smith, Dayle MA, and Rosso, Kevin M. Possible Dynamically Gated Conductance along Heme Wires in Bacterial Multiheme Cytochromes. United States: N. p., 2014. Web. doi:10.1021/jp502803y.
Smith, Dayle MA, & Rosso, Kevin M. Possible Dynamically Gated Conductance along Heme Wires in Bacterial Multiheme Cytochromes. United States. https://doi.org/10.1021/jp502803y
Smith, Dayle MA, and Rosso, Kevin M. 2014. "Possible Dynamically Gated Conductance along Heme Wires in Bacterial Multiheme Cytochromes". United States. https://doi.org/10.1021/jp502803y.
@article{osti_1172458,
title = {Possible Dynamically Gated Conductance along Heme Wires in Bacterial Multiheme Cytochromes},
author = {Smith, Dayle MA and Rosso, Kevin M.},
abstractNote = {The staggered cross decaheme configuration of electron transfer co-factors in the outer-membrane cytochrome MtrF may serve as a prototype for conformationally-gated multi-heme electron transport. Derived from the bacterium Shewanella oneidensis, the staggered cross configuration reveals intersecting c-type octaheme and tetraheme “wires” containing thermodynamic “hills” and “valleys”, suggesting that the protein structure may include a dynamical mechanism for conductance and pathway switching depending on enzymatic functional need. Recent molecular simulations have established the pair-wise electronic couplings, redox potentials, and reorganization energies to predict the maximum conductance along the various heme wire pathways by sequential hopping of a single electron (PNAS (2014) 11,611-616). Here, we expand this information with classical molecular and statistical mechanics calculations of large-amplitude protein dynamics in MtrF, to address its potential to modulate pathway conductance, including assessment of the effect of the total charge state. Explicit solvent molecular dynamics simulations of fully oxidized and fully reduced MtrF employing ten independent 50-ns simulations at 300 K and 1 atm showed that reduced MtrF is more expanded and explores more conformational space than oxidized MtrF, and that heme reduction leads to increased heme solvent exposure. The slowest mode of collective decaheme motion is 90% similar between the oxidized and reduced states, and consists primarily of inter-heme separation with minor rotational contributions. The frequency of this motion is 1.7×107 s 1 for fully-oxidized and fully-reduced MtrF, respectively, slower than the downhill electron transfer rates between stacked heme pairs at the octaheme termini and faster than the electron transfer rates between parallel hemes in the tetraheme chain. This implies that MtrF uses slow conformational fluctuations to modulate electron flow along the octaheme pathway, apparently for the purpose of increasing the residence time of electrons on lowest potential hemes 4 and 9. This apparent gating mechanism should increase the success rate of electron transfer from MtrF to low potential environmental acceptors via these two solvent-exposed hemes.},
doi = {10.1021/jp502803y},
url = {https://www.osti.gov/biblio/1172458}, journal = {Journal of Physical Chemistry B, 118(29):8505–8512},
number = ,
volume = ,
place = {United States},
year = {Thu Jul 24 00:00:00 EDT 2014},
month = {Thu Jul 24 00:00:00 EDT 2014}
}