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

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.

Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii

“…1D and 2C). The spatial organization of heme_2 to heme_5 resembles that of the tetraheme in Shewanella oneidensis STC, in which the electron transfer between stacked heme pairs is approximately an order of magnitude greater than for the T-shaped heme pairs (25). But the electronic coupling of T-shaped heme pairs would be strongly enhanced by cysteine linkages inserted in the space between these pairs (26).…”

Examination of abiotic cofactor assembly in photosynthetic biomimetics: site-specific stereoselectivity in the conjugation of a ruthenium(II) tris(bipyridine) photosensitizer to a multi-heme protein

“…More recent work shows possibilities to create conjugates with even faster ET rates (Kokhan et al 2017). Further, ultrafast PET has also been demonstrated in tetraheme heme protein architectures (van Wonderen et al 2019). The cases of PET occurring on the few ps timescale are remarkable because these reactions begin to mimic the primary photosynthetic electron transfer steps and regarded as a goal for the design of biomimetic hybrids.…”

Ergodicity Breaking in Thermal Biological Electron Transfer? Cytochrome C Revisited II

“…What becomes clear from many simulation studies in our group is that the effect of electronic polarization of the environment (here protein and water) needs to be included in the calculations. 1,17,[44][45][46][47][48][49][50][51] Otherwise reorganization free energy is strongly overestimated compared to experimentally determined values from photoemission spectroscopy and electrochemistry, not only for proteins but also for simple aqueous transition metal ion complexes Ru(bpy)…”