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 <i>Bryopsis corticulans</i> 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 <i>Bry. corticulans</i> (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 <i>Bry. corticulans</i> and spinach are compared.