Dynamic changes between two LHCX-related energy quenching sites control diatom photoacclimation

Marine diatoms are prominent phytoplankton organisms, optimally performing photosynthesis in extremely variable environments. Diatoms possess a strong ability to dissipate excess absorbed energy as heat via non-photochemical quenching (NPQ). This process relies on changes in carotenoid pigment composition (xanthophyll cycle) and on specific members of the light-harvesting complex (LHC) family specialized in photoprotection (LHCX), which potentially act as NPQ effectors. However, the link between light stress, NPQ, and the existence of different LHCX isoforms is not understood in these organisms. Using picosecond fluorescence analysis, we observed two types of NPQ in the pennate diatom Phaeodactylum tricornutum, depending on light conditions. Short exposure of low-light acclimated cells to high light triggers the onset of energy quenching close to the core of Photosystem II, while prolonged light stress activates NPQ in the antenna. Biochemical analysis indicates a link between the changes in the NPQ site/mechanism and the induction of different LHCX isoforms, which accumulate either in the antenna complexes or in the core complex. By comparing the responses of WT cells and of transgenic lines with a reduced expression of the major LHCX isoform (lhcx1), we conclude that core-complex-associated NPQ is more effective in photoprotection than the antenna one. Overall, our data clarify the complex molecular scenario of light responses in diatoms, and provide a rationale for the existence of a degenerate family of LHCX proteins in these algae.