Abstract
Multiheme cytochromes attract much attention for their electron transport properties. These proteins conduct electrons across bacterial cell walls and along extracellular filaments and when purified can serve as bionanoelectronic junctions. Thus, it is important and necessary to identify and understand the factors governing electron transfer in this family of proteins. To this end we have used ultrafast transient absorbance spectroscopy, to define heme-heme electron transfer dynamics in the representative multiheme cytochrome STC from Shewanella oneidensis in aqueous solution. STC was photosensitized by site-selective labeling with a Ru(II)(bipyridine)3 dye and the dynamics of light-driven electron transfer described by a kinetic model corroborated by molecular dynamics simulation and density functional theory calculations. With the dye attached adjacent to STC Heme IV, a rate constant of 87 × 106 s-1 was resolved for Heme IV → Heme III electron transfer. With the dye attached adjacent to STC Heme I, at the opposite terminus of the tetraheme chain, a rate constant of 125 × 106 s-1 was defined for Heme I → Heme II electron transfer. These rates are an order of magnitude faster than previously computed values for unlabeled STC. The Heme III/IV and I/II pairs exemplify the T-shaped heme packing arrangement, prevalent in multiheme cytochromes, whereby the adjacent porphyrin rings lie at 90° with edge-edge (Fe-Fe) distances of ∼6 (11) Å. The results are significant in demonstrating the opportunities for pump-probe spectroscopies to resolve interheme electron transfer in Ru-labeled multiheme cytochromes.
Highlights
Species of Shewanella attract much interest for their ability to respire in the absence of oxygen by transferring electrons from intracellular oxidation of organic matter to extracellular acceptors including Fe2O3 and MnO2 nanoparticles.[1,2] Multiheme cytochromes are essential to this process, and these fascinating proteins are spanned by chains of close-packed ctype hemes
The STC heme II/III pair exemplifies the stacked packing motif with parallel porphyrin rings in van der Waals contact and a shorter edge− edge (Fe−Fe) distance of ∼4 (∼9) Å. The possibility that these geometries are optimized to impose control over electron transfer rates and direction has been explored at a singleprotein level through quantum chemistry and molecular simulation.[17−21] to the best of our knowledge, direct measurements of heme−heme electron transfer rates have yet to be reported for STC or other multiheme cytochromes
Features in the transient absorbance (TA) are assigned to states within the photocycle of Scheme 1 and their transient populations accurately reproduced by a kinetic model that extends Scheme 1 to include electron transfer across the Heme IV ↔ Heme III pair
Summary
Species of Shewanella attract much interest for their ability to respire in the absence of oxygen by transferring electrons from intracellular oxidation of organic matter to extracellular acceptors including Fe2O3 and MnO2 nanoparticles.[1,2] Multiheme cytochromes are essential to this process, and these fascinating proteins are spanned by chains of close-packed ctype hemes. The STC heme II/III pair exemplifies the stacked packing motif with parallel porphyrin rings in van der Waals contact and a shorter edge− edge (Fe−Fe) distance of ∼4 (∼9) Å The possibility that these geometries are optimized to impose control over electron transfer rates and direction has been explored at a singleprotein level through quantum chemistry and molecular simulation.[17−21] to the best of our knowledge, direct measurements of heme−heme electron transfer rates have yet to be reported for STC or other multiheme cytochromes. A nonergodicity correction to the reorganization free energy was applied as recommended[42] to account for the ultrafast time-scale of the experiments described here To this end we applied the self-consistent iteration scheme suggested previously,[17] where the outer-sphere contributions that are slower than the actual electron transfer event are removed, see Figure S11. MD simulations, and calculation of electron transfer parameters can be found in the Supporting Information
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