Coupled rows of PBS cores and PSII dimers in cyanobacteria: symmetry and structure

Abstract

Phycobilisome (PBS) is a giant water-soluble photosynthetic antenna transferring the energy of absorbed light mainly to the photosystem II (PSII) in cyanobacteria. Under the low light conditions, PBSs and PSII dimers form coupled rows where each PBS is attached to the cytoplasmic surface of PSII dimer, and PBSs come into contact with their face surfaces (state 1). The model structure of the PBS core that we have developed earlier by comparison and combination of different fine allophycocyanin crystals, as reported in Zlenko et al. (Photosynth Res 130(1):347-356, 2016b), provides a natural way of the PBS core face-to-face stacking. According to our model, the structure of the protein-protein contact between the neighboring PBS cores in the rows is the same as the contact between the APC hexamers inside the PBS core. As a result, the rates of energy transfer between the cores can occur, and the row of PBS cores acts as an integral PBS "supercore" providing energy transfer between the individual PBS cores. The PBS cores row pitch in our elaborated model (12.4 nm) is very close to the PSII dimers row pitch obtained by the electron microscopy (12.2 nm) that allowed to unite a model of the PBS cores row with a model of the PSII dimers row. Analyzing the resulting model, we have determined the most probable locations of ApcD and ApcE terminal emitter subunits inside the bottom PBS core cylinders and also revealed the chlorophyll molecules of PSII gathering energy from the PBS.

Rates and pathways of energy migration from the phycobilisome to the photosystem II and to the orange carotenoid protein in cyanobacteria

“…The architecture of the PBS‐PSII‐RCP supercomplex was based on the PBS core model developed according to the structure of the lattice of several different APC crystals and the restrictions on the PBS core cylinders' length resulting from the vast amount of the EM observations ; the X‐ray structures of the PSII dimer from Thermosynechococcus elongatus (PDB ID: http://www.rcsb.org/pdb/search/structidSearch.do?structureId=4PJO, ); and the proteolytically cleaved N‐terminal domain of OCP from Synechocystis sp. PCC 6803 (RCP, PDB ID: http://www.rcsb.org/pdb/search/structidSearch.do?structureId=4XB4, ).…”

“…Some of the existing molecular models of the OCP‐PBS complex propose the distortion of the PBS, including the limited dissociation of the APC trimers of the PBS core . Some other models obtained for the whole OCP globule and its N‐terminal domain did not imply any PBS structure alterations and appeared to be very similar with regard to the hECN and ApcE phycobilin mutual orientation. These models imply that the N‐terminal domain interacts with the concaved surface of the tip on the side of the APC trimer close to the ApcE chromophore.…”

“…At a room temperature, the 660 nm fluorescence emission appears as a result of the backward energy transfer from 680 nm chromophores . Still, the arrangement of the subunits in the PBS basal cylinders has not been determined unambiguously , and the ApcE and ApcD can be located in the neighboring or remote APC trimers . The energy of the absorbed light migrates down the peripheral rods to the bulk APC, then to the TEs and finally—to the antennal chlorophyll of PSII.…”

“…Some structural details were revealed by cryo‐EM and cross‐linking/mass‐spectrometry techniques , but their resolution was not sufficient to calculate energy transfer. Therefore, at present the effective way to study the PBS‐PSII supercomplex formation and function is limited to spatial modeling based on the existing crystallographic and EM data .…”

“…The molecular mechanism of OCP action has to be very fast to compete with the energy transfer from PBS to PSII. To assess the rates of excitation energy transfer in the cyanobacterial light‐harvesting system, we have used a molecular model of the triple complex of the PBS core, PSII dimer, and RCP . The energy transfer from PBS to PSII was validated using the Förster resonance energy transfer (FRET) theory , while the energy transfer from PBS to OCP was calculated with the excitonic theory .…”