Lipid Membrane Regulation of Chlorophyll Triplet Excitation Quenching in Photosynthetic Light-Harvesting Complex LHCII

Carotenoid (Car) in photosynthesis plays an essential role in photoprotection by quenching chlorophyll triplet excitation (3Chl*) via a Chl-to-Car triplet energy transfer (TET). However, mechanistic studies on the Car triplet photoprotection (CTP) have been complicated by the involvement of the O2 quenching and the complexity of the thylakoid membrane. To clarify the interplay of the TET with the effects of O2 and lipid–protein interaction, we prepared nanodiscoidal lipid–protein assemblies of the light-harvesting complexes of photosystem II (LHCII) of Bryopsis corticulans and spinach and examined their triplet excitation dynamics in a broad temporal regime of 1–105 ns. For both kinds of LHCII complexes, besides the well-known ultrafast TET at both L1 and L2 sites, an O2 insensitive, slow TET reaction at the L1 (but not L2) site proceeding with a time constant of 11–25 ns was verified. Lipid membranes can substantially accelerate the slow TET reaction and prolong the 3Car* lifetime. On the other hand, both kinds of LHCII complexes bear a minor fraction of Car-unquenchable 3Chl*, i.e., 2.2% and 4.6% (1.5% and 2.2%) for Bry. corticulans (spinach) LHCII complexes in lipid and aqueous phases, respectively, which can be fully quenched by O2. In addition, the lipid membrane promotes the O2 accessibility of LHCII proteins and, compared to L2, the L1 site is (30–130)% more permissive to O2 access. The heterogeneous 3Chl* deactivation pathways and CTP potency of Bry. corticulans and spinach are compared.