Trimeric Photosystem I facilitates energy transfer from phycobilisomes in Synechocystis PCC 6803

In cyanobacteria, phycobilisomes serve as peripheral light-harvesting complexes of the two photosystems, extending their antenna size and the wavelength range of photons available for photosynthesis. The abundance of phycobilisomes, the number of phycobiliproteins they contain, and their light-harvesting function are dynamically adjusted in response to the physiological conditions. Phycobilisomes are also thought to be involved in state transitions that maintain the excitation balance between the two photosystems. Unlike its eukaryotic counterpart, PSI is trimeric in many cyanobacterial species and the physiological significance of this is not well understood. Here we compared the composition and light-harvesting function of phycobilisomes in cells of Synechocystis PCC 6803, which has primarily trimeric PSI, and the ΔpsaL mutant unable to form trimers. We also investigated a mutant additionally lacking the PsaJ and PsaF subunits of PSI, as PsaF has been proposed to facilitate interaction with phycobilisomes. Both strains with monomeric PSI accumulated significantly less phycocyanin (which constitutes the phycobilisome rods) per chlorophyll, while the allophycocyanin content was unchanged compared to WT. These data show that cells with monomeric PSI have higher abundance of smaller phycobilisomes. Steady-state and time-resolved fluorescence spectroscopy at room temperature and 77 K revealed that PSII receives more energy from the phycobilisomes at the expense of PSI in cells with monomeric PSI, regardless of the presence of PsaF. Taken together, these results show that the trimeric organization of PSI is advantageous for efficient and balanced excitation energy transfer from phycobilisomes in Synechocystis . One-sentence summary Cyanobacterial mutants with monomeric PSI have higher abundance of smaller phycobilisomes transferring more energy to PSII than to PSI, thus trimeric PSI is important for balanced energy flow.