Molecular computational investigation of electron-transfer kinetics across cytochrome - Iron oxide interfaces

Sebastien Kerisit, Kevin M. Rosso, Michel Dupuis, Marat Valiev

Research output: Contribution to journalArticle

47 Citations (Scopus)

Abstract

The interface between electron-transfer proteins such as cytochromes and solid-phase mineral oxides is central to the activity of dissimilatory-metal reducing bacteria. A combination of potential-based molecular dynamics simulations and ab initio electronic structure calculations are used in the framework of Marcus's electron-transfer theory to compute elementary electron-transfer rates from a well-defined cytochrome model, namely, the small tetraheme cytochrome (STC) from Shewanella oneidensis, to surfaces of the iron oxide mineral hematite (α-Fe2O3). Room-temperature molecular dynamics simulations show that an isolated STC molecule favors surface attachment via direct contact of hemes I and IV at the poles of the elongated axis, with electron-transfer distances as small as 9 Å. The cytochrome remains attached to the mineral surface in the presence of water and shows limited surface diffusion at the interface. Ab initio electronic coupling matrix element (VAB) calculations of configurations excised from the molecular dynamics simulations reveal VAB values ranging from 1 to 20 cm-1, consistent with nonadiabaticity. Using these results, together with experimental data on the redox potential of hematite and hemes in relevant cytochromes and calculations of the reorganization energy from cluster models, we estimate the rate of electron transfer across this model interface to range from 1 to 1000 s-1 for the most exothermic driving force considered in this work and from 0.01 to 20 s-1 for the most endothermic. This fairly large range of electron-transfer rates highlights the sensitivity of the rate upon the electronic coupling matrix element, which is in turn dependent on the fluctuations of the heme configuration at the interface. We characterize this dependence using an idealized bisimidazole heme to compute from first principles the VAB variation due to porphyrin ring orientation, electron-transfer distance, and mineral surface termination. The electronic matrix element and consequently the rate of electron transfer are found to be sensitive to all parameters considered. This work indicates that biomolecularly similar solvent-exposed bishistidine hemes in outer-membrane cytochromes such as MtrC or OmcA are likely to have an affinity for the oxide surface in water governing the approach and interfacial conformation and, if allowed sufficient conformational freedom, will achieve distances and configurations required for direct interfacial electron transfer.

Original languageEnglish
Pages (from-to)11363-11375
Number of pages13
JournalJournal of Physical Chemistry C
Volume111
Issue number30
DOIs
Publication statusPublished - Aug 2 2007

Fingerprint

cytochromes
Cytochromes
Iron oxides
iron oxides
electron transfer
Proteins
Kinetics
Electrons
Heme
kinetics
minerals
Oxide minerals
Molecular dynamics
Hematite
hematite
molecular dynamics
Minerals
Computer simulation
matrices
configurations

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Electronic, Optical and Magnetic Materials
  • Surfaces, Coatings and Films
  • Energy(all)

Cite this

Molecular computational investigation of electron-transfer kinetics across cytochrome - Iron oxide interfaces. / Kerisit, Sebastien; Rosso, Kevin M.; Dupuis, Michel; Valiev, Marat.

In: Journal of Physical Chemistry C, Vol. 111, No. 30, 02.08.2007, p. 11363-11375.

Research output: Contribution to journalArticle

Kerisit, Sebastien ; Rosso, Kevin M. ; Dupuis, Michel ; Valiev, Marat. / Molecular computational investigation of electron-transfer kinetics across cytochrome - Iron oxide interfaces. In: Journal of Physical Chemistry C. 2007 ; Vol. 111, No. 30. pp. 11363-11375.
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abstract = "The interface between electron-transfer proteins such as cytochromes and solid-phase mineral oxides is central to the activity of dissimilatory-metal reducing bacteria. A combination of potential-based molecular dynamics simulations and ab initio electronic structure calculations are used in the framework of Marcus's electron-transfer theory to compute elementary electron-transfer rates from a well-defined cytochrome model, namely, the small tetraheme cytochrome (STC) from Shewanella oneidensis, to surfaces of the iron oxide mineral hematite (α-Fe2O3). Room-temperature molecular dynamics simulations show that an isolated STC molecule favors surface attachment via direct contact of hemes I and IV at the poles of the elongated axis, with electron-transfer distances as small as 9 {\AA}. The cytochrome remains attached to the mineral surface in the presence of water and shows limited surface diffusion at the interface. Ab initio electronic coupling matrix element (VAB) calculations of configurations excised from the molecular dynamics simulations reveal VAB values ranging from 1 to 20 cm-1, consistent with nonadiabaticity. Using these results, together with experimental data on the redox potential of hematite and hemes in relevant cytochromes and calculations of the reorganization energy from cluster models, we estimate the rate of electron transfer across this model interface to range from 1 to 1000 s-1 for the most exothermic driving force considered in this work and from 0.01 to 20 s-1 for the most endothermic. This fairly large range of electron-transfer rates highlights the sensitivity of the rate upon the electronic coupling matrix element, which is in turn dependent on the fluctuations of the heme configuration at the interface. We characterize this dependence using an idealized bisimidazole heme to compute from first principles the VAB variation due to porphyrin ring orientation, electron-transfer distance, and mineral surface termination. The electronic matrix element and consequently the rate of electron transfer are found to be sensitive to all parameters considered. This work indicates that biomolecularly similar solvent-exposed bishistidine hemes in outer-membrane cytochromes such as MtrC or OmcA are likely to have an affinity for the oxide surface in water governing the approach and interfacial conformation and, if allowed sufficient conformational freedom, will achieve distances and configurations required for direct interfacial electron transfer.",
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