Novel Features of Eukaryotic Photosystem II Revealed by Its Crystal Structure Analysis from a Red Alga

Abstract

Photosystem II (PSII) catalyzes light-induced water splitting, leading to the evolution of molecular oxygen indispensible for life on the earth. The crystal structure of PSII from cyanobacteria has been solved at an atomic level, but the structure of eukaryotic PSII has not been analyzed. Because eukaryotic PSII possesses additional subunits not found in cyanobacterial PSII, it is important to solve the structure of eukaryotic PSII to elucidate their detailed functions, as well as evolutionary relationships. Here we report the structure of PSII from a red alga Cyanidium caldarium at 2.76 Å resolution, which revealed the structure and interaction sites of PsbQ, a unique, fourth extrinsic protein required for stabilizing the oxygen-evolving complex in the lumenal surface of PSII. The PsbQ subunit was found to be located underneath CP43 in the vicinity of PsbV, and its structure is characterized by a bundle of four up-down helices arranged in a similar way to those of cyanobacterial and higher plant PsbQ, although helices I and II of PsbQ were kinked relative to its higher plant counterpart because of its interactions with CP43. Furthermore, two novel transmembrane helices were found in the red algal PSII that are not present in cyanobacterial PSII; one of these helices may correspond to PsbW found only in eukaryotic PSII. The present results represent the first crystal structure of PSII from eukaryotic oxygenic organisms, which were discussed in comparison with the structure of cyanobacterial PSII.Oxygenic photosynthesis provides us with food, oxygen, and fuel and is therefore vital to life on the earth. The first reaction occurring in oxygenic photosynthesis is the splitting of water into electrons, protons, and molecular oxygen, among which electrons and protons are utilized for the synthesis of NADPH and ATP, whereas oxygen is supplied to the atmosphere for maintaining aerobic life forms. The water splitting reaction is catalyzed by photosystem II (PSII), 5 an extremely large membrane-protein complex located in thylakoid membranes from prokaryotic cyanobacteria to higher plants. In the case of cyanobacteria, the crystal structure of PSII has been solved with its resolution gradually increased to an atomic level of 1.9 Å (1-6), which showed that PSII contains 17 transmembrane subunits and 3 peripheral, hydrophilic subunits with a total molecular mass of 700 kDa for a dimer.The first oxygenic photosynthetic organism is believed to be the ancestor of cyanobacteria some 2.7 billion years ago (7). Although the subunit compositions of PSII from cyanobacteria to higher plants we see today are rather conserved, some apparent differences exist in both the transmembrane and peripheral subunits among cyanobacteria, various algae, and higher plants (8). One of the remarkable differences is found in the composition and function of extrinsic proteins associated in the lumenal side and required for maintaining the optimal function of the water-splitting reaction. In cyanobacteria, three extrinsic proteins of PsbO (33 kDa), Ps...

Functional role of Lys residues of Psb31 in electrostatic interactions with diatom photosystem II

“…In the previous chemical modification study [21], it was proposed that PsbE and/or PsbH subunits were possible binding partners of Psb31 based on both the previous suggestion of cross-linking and mass spectrometry experiments [18] and the red algal PSII structure [25]. As observed on the lumenal side of red algal PSII [25], PsbE and PsbH have at least nine and three negatively charged amino acids including the C termini, respectively, suggesting that the negatively charged amino acids in PsbE and PsbH are plausible binding sites with Lys39/Lys54/Lys57 in addition to Lys33/Lys56/Lys69 of Psb31.…”

Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution

“…7), whereas PsbW is present only in higher plants and algae but not in cyanobacteria 20 . In red algal PSII (CcPSII from Cyanidium caldarium) 21 , a subunit found at a location adjacent to PsbI and named 'chain S' may correspond to spinach PsbW. PsbZ is the only subunit with two transmembrane helices and its N and C termini are both positioned on the luminal surface, whereas the other 11 subunits all have a single transmembrane helix.…”

The singular properties of photosynthetic cytochrome c550 from the diatom Phaeodactylum tricornutum suggest new alternative functions

“…It is important to note that most proteins that co‐immunoseparated in the crosslinked fraction have been already annotated as being located in the chloroplast (Figs and S3), validating the reliability of the method used. In addition to several PSII subunits (Psb31, CP43, D1 and D2), expected from the Cc 550 location in the red algal PSII structure (Ago et al ), only a very limited number of proteins co‐immunoseparated in the three types of samples analyzed (Fig. ), including RubisCO (large and small subunits) and PtCA1 (a ß‐CA), both located in the pyrenoid compartment (Satoh et al , Tachibana et al , Kikutani et al 2016).…”

“…According to the PSII known structures, the facing surface of Cc 550 (Fig. ), that includes the cofactor exposed area, is involved in the binding to the photosystem, maintaining close contacts with the PSII surface (Ago et al ). Consequently, the distinctive surface charge distribution of eukaryotic Cc 550 could be significant when establishing the binding affinity to PSII, as previously suggested for the P. tricornutum Cc 550 (Bernal‐Bayard et al ).…”