Second-Sphere Protonation Imparts a Biologically Relevant Potential Shift in a Chlorophyll Model Compound

Electrostatic protein-pigment interactions have been implicated in tuning the electron transfer chemistry of chlorophylls in vivo; however, these effects are difficult to probe directly, leading to a dearth of experimental data that limits our understanding. Herein, we report a chlorophyll model compound based on a Mg-porphyrin framework with a secondary coordination sphere designed to probe isolated electrostatic interactions with the porphyrin macrocycle. Protonation of two second-sphere amine groups led to a significant increase in the redox potential of the porphyrin ring, drawing a strong analogy to the postulated influence of protonated amino acids on the properties of chlorophylls in vivo. Experimental techniques (electronic absorption spectroscopy, single-crystal X-ray diffraction, cyclic voltammetry) were complemented by density functional theory calculations to uncover the impact of the proximal charged substituents on the electronic structure of the Mg-porphyrin complex. 1-electron oxidation of the protonated complex yielded the corresponding π-cation radical complex, which mimicked the reaction between photo-oxidized chlorophyll and tyrosine during photosynthesis by rapidly oxidizing phenolic substrates to yield phenoxyl radicals via electron-transfer-limited proton-coupled electron transfer. Overall, this work lends strong experimental support for the role of local protein electrostatics in achieving high-potential chlorophyll-based oxidants in Nature.