Structural modeling of the phycobilisome core and its association with the photosystems

Abstract

The phycobilisome (PBS) is a major light-harvesting complex in cyanobacteria and red algae. To obtain the detailed structure of the hemidiscoidal PBS core composed of allophycocyanin (APC) and minor polypeptide components, we analyzed all nine available 3D structures of APCs from different photosynthetic species and found several variants of crystal packing that potentially correspond to PBS core organization. Combination of face-to-face APC trimer crystal packing with back-to-back APC hexamer packing suggests two variants of the tricylindrical PBS core. To choose one of these structures, a computational model of the PBS core complex and photosystem II (PSII) dimer with minimized distance between the terminal PBS emitters and neighboring antenna chlorophylls was built. In the selected model, the distance between two types of pigments does not exceed 37 Å corresponding to the Förster mechanism of energy transfer. We also propose a model of PBS and photosystem I (PSI) monomer interaction showing a possibility of supercomplex formation and direct energy transfer from the PBS to PSI.

Structure of cyanobacterial phycobilisome core revealed by structural modeling and chemical cross-linking

“…The detailed structural orientation of the PBS and the RCs, however, remains to be determined, probably because of the structurally weak interactions of PBS and RCs, which could be advantageous for easy regulation of the excitation energy transfer under varying light conditions (5,6). The PBS core not only serves as a cornerstone for the rods to attach (7,8) but also acts as an anchoring module that enables efficient energy flow from PBSs to RCs (9)(10)(11)(12)(13).…”

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

“…In each PBS core basal cylinder, four phycobilin chromophores in corresponding APC trimers (Fig. ) are close to the bottom surface of the whole PBS , and we will refer to them as ‘bottom’ phycobilins. These phycobilins appear to be the closest to the cytoplasmic side of PSII and its chlorophylls.…”

“…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 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 natural design for harvesting far-red light: the antenna increases both absorption and quantum efficiency of Photosystem II

“…Not only is Chl505 the most strongly coupled pigment to ChlD1, it is also located at the stromal side of the complex, where the PBS basal core cylinder attaches to PSII. Furthermore, structural data/models of supercomplexes of PBS and (Chl a-only) PSII, indicate that the terminal emitters of the PBS, located in the ApcE subunit, are spatially closer to the Chls of CP43 than those of CP47 8,34 . Finally, the weak connectivity between the Chls of CP43 and those of CP47 could account for the dependency of the fluorescence spectra on the excitation wavelength.…”