Ultrafast Light-Driven Electron Transfer in a Ru(II)tris(bipyridine)-Labelled Multiheme Cytochrome

Jessica H. van Wonderen, Christopher R. Hall, Xiuyun Jiang, Katrin Adamczyk, Antoine Carof, Ismael Heisler, Samuel E. H. Piper, Thomas A. Clarke, Nicholas J. Watmough, Igor V. Sazanovich, Michael Towrie, Stephen R. Meech (Lead Author), Jochen Blumberger (Lead Author), Julea N. Butt (Lead Author)

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Abstract

Multiheme cytochromes attract much attention for their electron transport properties. These proteins conduct electrons across bacterial cell walls, 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 ultra-fast transient absorbance spectroscopy, to define heme-heme electron transfer dynamics in the representative multiheme cytochrome STC from Shewanella oneidensis in aqueous solution. STC was photo-sensitized by site-selective labelling 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 x 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 x 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 90o with edge-edge (Fe-Fe) distances of ≈6 (11) Å. The results are significant in demonstrating the opportunities for pump-probe spectroscopies to resolve inter-heme electron transfer in Ru-labeled multiheme cytochromes.
Original languageEnglish
Pages (from-to)15190-15200
Number of pages11
JournalJournal of the American Chemical Society
Volume141
Issue number38
Early online date27 Aug 2019
DOIs
Publication statusPublished - 25 Sep 2019

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