Uphill energy transfer mechanism for photosynthesis in the Antarctic alga

Abstract

Prasiola crispa, a major green alga in Antarctica, forms layered colonies for survival under the severe terrestrial conditions of Antarctica, which include severe cold, drought, and strong sunlight. As a result of these conditions, the surface cells of P. crispa and other Antarctic organisms face high risk of photodamage. Cells of deeper layer escape from photodamage at the sacrifice of photosynthetic active radiation except infrared. P. crispa achieves effective photosynthesis by low energy far-red light for photosystem II excitation with high efficiency similar to that of visible light. Here, we identified a far-red light-harvesting complex of photosystem II in P. crispa, Pc-frLHC, and proposed a molecular mechanism of uphill excitation energy transfer based on its cryogenic electron-microscopy structure. While Pc-frLHC is associated with photosystem II, it is evolutionarily related to the light-harvesting complex of photosystem I. Pc-frLHC forms a ring-shaped homo-undecamer in which all chlorophyll a molecules are energetically connected and contains chlorophyll a trimers. It seems that the trimers are long-wavelength-absorbing chlorophylls for far-red light at 708 nm, and further absorbance extension is accomplished by Davydov-splitting in dimeric chlorophylls. The chlorophyll network should enable a highly efficient entropy-driven uphill excitation energy transfer using far-red light up to 725 nm.