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bioRxiv · 10.1101/2025.09.06.674587

Evolutionary origin and functional mechanism of Lhcx in the diatom photoprotection

Kumazawa, M.·Akimoto, S.·Takabayashi, A.·Imaizumi, K.·Tsuji, S.·Hasegawa, H.·Sakurai, A.·Imamura, S.·Ishikawa, N.·Inoue-Kashino, N.·Kashino, Y.·Ifuku, K.
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Abstract

Diatoms are red-lineage algae that utilize the light-harvesting complex (LHC) subfamily Lhcx for photoprotection via non-photochemical quenching (NPQ); however, its evolutionary origin and molecular mechanism remain poorly understood. Through molecular phylogenetic analysis, we show that diatom Lhcxs and green algal Lhcsrs evolved from a common ancestor, with green plants subsequently acquiring them via horizontal gene transfer. To investigate the functional role of Lhcx1, we generated knockout mutants of Chaetoceros gracilis, a diatom with low Lhcx redundancy. The lhcx1 mutants nearly abolished NPQ, and time-resolved fluorescence measurements revealed that Lhcx1-mediated quenching occurs in energetically detached antenna complexes. Clear-native PAGE with Amphipol further indicated that CgLhcx1 interacts with the FCP L-dimer, functioning as a peripheral antenna for the C2S2M2 PSII-FCPII supercomplex. Notably, under high-light acclimation, lhcx1 mutants exhibited higher PSII effective quantum yields than wild type, attributable to reduced antenna size and enhanced carbon fixation capacity. The absence of NPQ accelerated high-light acclimation and was accompanied by increased xanthophyll accumulation, indicating that compensatory mechanisms can enhance overall photosynthetic efficiency. Together, these findings reveal the evolutionary origin of Lhcx/Lhcsr proteins and define the molecular basis of Lhcx1-mediated photoprotection in diatoms, providing fundamental insights into LHC-based photoprotection across photosynthetic lineages.

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Kumazawa, M., Akimoto, S., Takabayashi, A., Imaizumi, K., Tsuji, S., Hasegawa, H., Sakurai, A., Imamura, S., Ishikawa, N., Inoue-Kashino, N., Kashino, Y., Ifuku, K.. 2025-09-07. Evolutionary origin and functional mechanism of Lhcx in the diatom photoprotection. https://doi.org/10.1101/2025.09.06.674587

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