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

Abstract

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.

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

“…In particular, mixing of high-lying CT states with exciton states redshifts the exciton energy 48,49 . Therefore, Chl-Chl CT states have been identified as responsible for red-shifted bands in the fluorescence spectra of LHCII 50,51 and other plant antenna complexes 52,53 . These "red states" are likely not directly related to excitation quenching 54 , but they can be seen as spectral signatures of quenched conformations 55 .…”

Complete mapping of energy transfer pathways in the plant light-harvesting complex Lhca4

“…Two-dimensional electronic spectroscopy (2DES) has proven to be a particularly useful technique to study photosynthetic complexes involving almost dark states such as CT states. [23][24][25][26][27][28][29][30]32 is able to directly Fig. 1 Protein structure and pigment organization of monomeric reconstituted Lhca4.…”

Recent advances in multidimensional ultrafast spectroscopy

“…The 2DEV spectra reveal that this is not the case and that the lowest energy exciton states of LHCII have a significant population localized on Chl- b moieties via the presence of a peak that on the ω 1 axes lies at 675 nm, but on the ω 3 probe axes associated with Chl- b C=O stretching vibrations. The 2DEV study of LHCII has inspired further 2DES experiments and a re-evaluation and modifications to the LHCII Hamiltonian [ 165 ].…”