Mimicking Natural Photosynthsis: Ultrafast Charge Transfer in PpcA Ru(bpy)3 Complexes

Abstract

Converting light energy into its electrochemical equivalent requires precise control and fine tuning of relevant kinetic and thermodynamic parameters, including primary charge separation. To this end, we developed a series of 22 cysteine mutants of PpcA, a 3-heme cytochrome from Geobacter sulfurreducens as a model system to study short distance photo-induced electron transfer. These proteins were successfully expressed in E.coli and isolated for covalent labeling with Ru(bpy)2(bpy-Br). Protein purity and successful posttranslational modifications were confirmed with HPLC-MS. Time-resolved nanosecond and ultrafast transient absorbance characterization was performed at Argonne National Laboratory (ANL) and identified 6 constructs with apparent photo-induced charge transfer time constants of 20 ps or faster, including 2 constructs with 1-2 ps time constants. The latter is a significant result as up to this point only natural photosynthetic systems demonstrated such a fast initial charge separation, while all artificial covalent constructs exhibited charge transfer rates 3 or more orders of magnitude slower. To understand molecular principles responsible for such a dramatic acceleration of electron transfer rates, we conducted small- and wide angle X-ray scattering data collection at the Advanced Photon Source at ANL. Further, we are currently attempting to obtain X-ray crystallographic and NMR structures of the ultrafast constructs. Finally, we performed triplicate 250-300 ns all-atom molecular dynamics simulations of all 6 ultrafast constructs. Based on the obtained results we conclude that that photo-induced ultrafast charge transfer requires van der Waals contact between heme vinyl groups and photosensitizers while contacts with propionates or short covalent donor-acceptor distances play a much less significant role.