Modified architecture of Photosystems I and II in Euglena gracilis

The conversion of sunlight into chemical energy by oxygenic photosynthesis underpins the survival of virtually all life forms. The in-series activity of photosystems I (PSI) and II (PSII) mediates the linear transfer of electrons from water, the initial electron donor, to NADPH, thereby generating the reducing power needed for CO2 fixation. Photosynthetic microeukaryotes that acquired their chloroplast by secondary endosymbiotic events (referred to as secondary algae) play a vital role in primary production in the aquatic environments, they have evolved to adapt to a wide range of environments and consequently the diversity of protein ortholog groups in algae is almost the double when compared with land plants or vertebrates 1. In the present study we characterized the photosystems from Euglena gracilis, a non-parasitic secondary green alga related to trypanosomes. Genomic and biochemical analyses revealed that PSII lacks canonical CP24 and CP26 minor antenna proteins. Single particle analysis from electron microscopy images revealed that the formation of the PSII core dimer in this organism is different compared to other plant species and cyanobacteria, by the presence of a larger gap at the interaction interface between the two PSII cores. In addition, the location of the three LHC trimers is different in the largest Euglena PSII supercomplex found here compared to the Chlamydomonas C2S2M2N2 supercomplex 2. A similar analysis revealed that, despite of lacking the conserved LHCA proteins and several small subunits (PSAG/H/I/K/L/O/P), Euglena has maintained an overall PSI structure very close to the one described in plants 3 by the acquisition of specific LHCII-like antenna proteins. In addition, PSI associates to an unusual 250 kDa protein antenna complex which has a 77K-fluorescence emission peak at 710 nm.