Evidence for coherent mixing of excited and charge-transfer states in the major plant light-harvesting antenna, LHCII.

LHCII, the major light harvesting antenna from plants, plays a dual role in photosynthesis. In low light it is a light-harvester, while in high light it is a quencher that protects the organism from photodamage. The switching mechanism between these two orthogonal conditions is mediated by protein dynamic disorder and photoprotective energy dissipation. The latter in particular is thought to occur in part via spectroscopically 'dark' states. We searched for such states in LHCII trimers from spinach, at both room temperature and at 77 K. Using 2D electronic spectroscopy, we explored coherent interactions between chlorophylls absorbing on the low-energy side of LHCII, which is the region that is responsible for both light-harvesting and photoprotection. 2D beating frequency maps allow us to identify four frequencies with strong excitonic character. In particular, our results show the presence of a low-lying state that is coupled to a low-energy excitonic state. We assign this to a mixed excitonic-charge transfer state involving the state with charge separation within the Chl a603-b609 heterodimer, borrowing some dipole strength from the Chl a602-a603 excited states. Such a state may play a role in photoprotection, in conjunction with specific and environmentally controlled realizations of protein dynamic disorder. Our identification and assignment of the coherences observed in the 2D frequency maps suggests that the structure of exciton states as well as a mixing of the excited and charge-transfer states is affected by coupling of these states to resonant vibrations in LHCII.