Hidden electronic states in Light-Harvesting Complex II

Bart van Oort, Pengqi Xu, Laura Roy, Roberta Croce
Vrije Universiteit Amsterdam, Biophysics of Photosynthesis, Boelelaan 1081, 1081 HV Amsterdam, The Netherlands

Light-harvesting complex II (LHCII) is pivotal both for collecting solar radiation for photosynthesis, and for protection against photodamage under high light intensities (via non-photochemical quenching, NPQ). The nature of the NPQ quencher remains debated.
We recently developed a new all-optical method to populate a quenched state in unquenched LHCII [1]. The state showed characteristic features of an excitonically coupled lutein (Lut1) and chlorophyll (Chl) a. With its 9-10 ps lifetime it could act as a strong competitor for photodamage and photochemical quenching.
We extended these experiments to different types of LHCII: monomeric/trimeric, different xanthophyll (Xan) compositions, species, pH, detergent, and produced with different wavelength laser pulses. In all cases a 10ps-lived XanChl a photoproduct is observed, establishing it as a conserved property of LHCII. Interestingly, when Xans other than Lut bind at the L1/L2 site, they also form excitonically coupled states with Chl a, suggesting special properties of the L1/L2 sites.
Additionally, we show that the state is also populated as part of the singlet-singlet annihilation process in trimeric LHCII, which may explain contradictory reports on the nature of the quencher LHCII aggregates [2,3].
We propose that the observed state is also present in vivo, but is usually scarcely accessible. A pathway to the state may open upon specific conformational changes (e.g. in response to high excitation density). The state will then form an efficient quenching channel. The state may also cause the fluorescence blinking observed in single LHCs, where a small sub-population is in an energetically higher state with access to a quencher.

References

[1] van Oort, van Grondelle, van Stokkum, J Phys Chem B 2015, 119, 5184-5193
[2] Ruban, Berera, Ilioaia, van Stokkum, Kennis, Pascal, van Amerongen, Robert, Horton, van Grondelle, Nature 2007, 450, 575-579