Structures of PSI-FCPI from Thalassiosira pseudonana in high light provide convergent evolution and light-adaptive strategies in diatom FCPIs

Diatoms achieve great survival success in the fluctuating oceanic environment, rely on fucoxanthin chlorophyll a/c-binding proteins (FCPs) to complete light harvesting and quenching, which provide about 20% primary productivity on earth. We report two cryo-electron microscopic structures of photosystem I (PSI) with 13 or 5 FCPIs respectively at 2.78 [A] and 3.20 [A] resolution from Thalassiosira pseudonana under high light conditions. 8 Lhcr FCPIs are found detached from the PSI-13FCPI supercomplex under high light conditions, remaining 5 FCPIs are stably combined with the PSI core including Lhcr3, RedCAP, Lhcq8, Lhcf10, and FCP3 subunits. The specific pigment network in this centric diatom T. pseudonana demonstrates a higher proportion of Chlorophylls a, diadinoxanthins, and diatoxanthins but fewer fucoxanthins compared with the huge PSI-FCPI from another centric diatom Chaetoceros gracilis, thus exhibiting more efficiency in energy transfer and dissipation among FCPI antennas. These results reveal the assembly mechanism of several types of peripheral FCPIs and corresponding light-adaptive strategies in T. pseudonana, as well as the convergent evolution of the diatoms PSI-FCPI structures.