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

2019, Journal of the American Chemical Society

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  10 6 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  10 6 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 o with edge-edge (Fe-Fe) distances of 6 (11) Å. The results are significant in demonstrating the opportunities for pumpprobe spectroscopies to resolve inter-heme electron transfer in Ru-labeled multiheme cytochromes. Introduction: 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 Fe 2 O 3 and MnO 2 nanoparticles. 1-2 Multiheme cytochromes are essential to this process and these fascinating proteins are spanned by chains of close-packed c-type hemes. Intra-and inter-cytochrome electron transfer occurs by complementary Fe(III)  Fe(II) transitions of neighboring sites 3-5 and in this way electrons are moved from the inner bacterial membrane, across the periplasm and outer membrane lipid bilayer to reach the cell exterior. Multiheme cytochromes also contribute to the conductivity of extracellular structures, often termed bacterial nanowires, which transfer electrons across distances greatly exceeding cellular dimensions. These structures for Shewanella oneidensis are multiheme cytochrome containing extensions of the bacterial outer membrane 6 and for Geobacter sulfurreducens are filaments 7-8 comprised of a polymerized multiheme cytochrome. Beyond their biological role, the remarkable electron transfer properties of multiheme cytochromes have stimulated interest in these proteins as novel bioelectronic junctions and devices. 9-12 Furthermore, these proteins underpin the wiring of bacteria to electrodes 1, 13-15 to produce electricity in mediator-less microbial fuel cells and valued chemicals by microbial