Photo/thermo bi-cube mechanism of proton-coupled electron transfer reaction catalyzed by plant light-dependent protochlorophyllide oxidoreductase

Light-dependent protochlorophyllide oxidoreductase (LPOR), one of the few natural light-dependent enzymes relies on the cofactor NADPH to catalyze the conversion of protochlorophyllide to chlorophyllide during chlorophyll biosynthesis. However, acquiring the specific details of LPOR photocatalysis mechanism is challenging, as the intermediate species are generally complex and the chemical steps of interest are often kinetically obscure. Herein, the photochemistry associated with the comprehensive mechanism of C17C18 bond photoreduction inside LPOR was investigated using all-atom molecular dynamics simulations and electronic structure calculations in conjunction with vibronically nonadiabatic proton-coupled electron transfer (PCET) theory. The calculated electronic excitation spectrum and potential energy surfaces demonstrated that the finely modulated optical gap in the LPOR active center facilitates hole-electron separation and intersystem crossing to access the triplet states, which promotes effective photoredox catalysis by LPOR. The electrostatic coupling nature of the charge transfer reactions was revealed by determining the reaction energy paths related to the active site configuration prior to and after the transfer. The entire reaction was ultimately described as hydrogen atom transfer and subsequent stepwise electron and proton transfer process. This work provides a new perspective on the photocatalysis PCET in enzymatic environment with biochemistry relevance.