Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants

The plant photosynthetic machinery quenches excess excitation energy to avoid photodamage. Here, via molecular dynamics and quantum chemical calculations, Cupellini et al. show that lutein/chlorophyll pairs in light-harvesting complex II can quench excess energy via a transient charge transfer state. The photosynthetic apparatus of higher plants can dissipate excess excitation energy during high light exposure, by deactivating excited chlorophylls through a mechanism called nonphotochemical quenching (NPQ). However, the precise molecular details of quenching and the mechanism regulating the quenching level are still not completely understood. Focusing on the major light-harvesting complex LHCII of Photosystem II, we show that a charge transfer state involving Lutein can efficiently quench chlorophyll excitation, and reduce the excitation lifetime of LHCII to the levels measured in the deeply quenched LHCII aggregates. Through a combination of molecular dynamics simulations, multiscale quantum chemical calculations, and kinetic modeling, we demonstrate that the quenching level can be finely tuned by the protein, by regulating the energy of the charge transfer state. Our results suggest that a limited conformational rearrangement of the protein scaffold could act as a molecular switch to activate or deactivate the quenching mechanism.