Identification and design principles of far-red-absorbing chlorophyll in the light-harvesting complex

Photosystem II from Prasiola crispa employs a unique ring-shaped undecameric light-harvesting complex (Pc-frLHC) in addition to the commonly observed minor monomeric and major trimeric LHCIIs. Each monomer of Pc-frLHC contains four transmembrane helices. In contrast to the typical three-helix LHCIIs that constitute for the peripheral light-harvesting antennas for photosystem II, Pc-frLHC carries chlorophylls capable of far-red absorption. Combining spectroscopic analyses with a quantum mechanical/molecular mechanical approach, we identified the far-red-absorbing chlorophyll(s) in Pc-frLHC, as well as its counterpart in another Trebouxiophyceae alga Coccomyxa sp. Obi (Co-frLHC). Spectroscopic analysis reveals that both complexes exhibit far-red-shifted absorption of chlorophylls at ∼710 nm. In the Pc-frLHC structure, the Chla 603-609 dimer exhibits the strongest excitonic coupling among all apparent chlorophyll dimers. This dimer also exhibits the largest excitation-induced permanent dipole moment along the axis connecting the two chlorophylls, reflecting the most pronounced charge-transfer character. Furthermore, Chla 609 forms the second strongest excitonically coupled dimer with Chla 708, further extending the absorption into the far-red region. The conserved spatial arrangement and orientation of the chlorophyll trimer in Co-frLHC suggest that the Chla 603-609-708 trimer, located in the same frLHC monomer unit, which is predominantly characterized by the Chla 603-609 dimer, provides the structural basis for the far-red absorption in frLHCs.