Structural basis for different types of hetero-tetrameric light-harvesting complexes in a diatom PSII-FCPII supercomplex

Abstract

Fucoxanthin chlorophyll (Chl) a/c-binding proteins (FCPs) function as light harvesters in diatoms. The structure of a diatom photosystem II-FCPII (PSII-FCPII) supercomplex have been solved by cryo-electron microscopy (cryo-EM) previously; however, the FCPII subunits that constitute the FCPII tetramers and monomers are not identified individually due to their low resolutions. Here, we report a 2.5 Å resolution structure of the PSII-FCPII supercomplex using cryo-EM. Two types of tetrameric FCPs, S-tetramer, and M-tetramer, are identified as different types of hetero-tetrameric complexes. In addition, three FCP monomers, m1, m2, and m3, are assigned to different gene products of FCP. The present structure also identifies the positions of most Chls c and diadinoxanthins, which form a complicated pigment network. Excitation-energy transfer from FCPII to PSII is revealed by time-resolved fluorescence spectroscopy. These structural and spectroscopic findings provide insights into an assembly model of FCPII and its excitation-energy transfer and quenching processes.

Mechanism of Absorption Wavelength Shift Depending on the Protonation State of the Acrylate Group in Chlorophyll c

“…Absorption wavelength shift and light intensity: (a) low-light conditionChl c is deprotonated at high pH; (b) high-light conditionChl c is protonated at low pH, and the Soret and Q bands of Chl c are red-shifted. The cofactor arrangement of the PSII–FCP complex structure is shown . Note that Chl c 1 -303 and -309 in the PSII–FCP complex structure correspond to Chl c 1 and Chl c 2 in the isolated FCP crystal structure, respectively.…”

“…Thus, the LUMO and the LUMO+1 are delocalized toward the acrylate moiety only when the acrylate moiety is protonated, leading to stabilizations of the LUMO and the LUMO+1 and an increase in the absorption wavelength (Figure 7c). Although Chlcs are located only on the stromal side in the FCP crystal structure from Phaeodactylum tricornutum (Figure 1b), 4 cryo-electron microscopic analysis showed that Chlcs are also located on the lumenal side of the photosystem II−FCP (PSII−FCP) complex structure from the diatom Chaetoceros gracilis 8 (Figure 8). In photosynthesis, protons are released toward the lumenal side of the thylakoid membrane of chloroplasts, and the pH values on the lumenal side decrease as the reaction proceeds.…”

“…Although Chl c s are located only on the stromal side in the FCP crystal structure from Phaeodactylum tricornutum (Figure b), cryo-electron microscopic analysis showed that Chl c s are also located on the lumenal side of the photosystem II–FCP (PSII–FCP) complex structure from the diatom Chaetoceros gracilis (Figure ). In photosynthesis, protons are released toward the lumenal side of the thylakoid membrane of chloroplasts, and the pH values on the lumenal side decrease as the reaction proceeds.…”

“…4 FCP belongs to the superfamily of transmembrane lightharvesting complex (LHC) proteins with low sequence similarity to the main LHCI and LHCII subunits of green lineage organisms, 5,6 although Chlcs in FCP are replaced with Chla or Chlb in LHCI and LHCII. 4,7 The number of fucoxanthin molecules is larger in FCP (five to seven in each monomer 4,8 ) than that of carotenoid molecules in LHCI and LHCII (three or four in each monomer subunit 4,9 ). Chlcs and fucoxanthin molecules in FCP are likely to contribute to the difference in absorption and dissipation features between FCP and LHCI/LHCII.…”

Origin of Energy Dissipation in the Oligomeric Fucoxanthin-Chlorophyll a/c Binding Proteins

“…Note that there are two types of FCP-A tetramer found in C. gracilis, one strongly associated (Stetramer) with the PSII core and the other moderately associated (M-tetramer), and only the latter one contains diadinoxanthin (Dd). 27 Thus, our sample of FCP-A represents more of the S-tetramer. The fluorescence emission spectra at 77 K (Figure 1C) of the two complexes exhibit large differences, with FCP-B/C emission peaking at 676 nm and FCP-A at 684 nm.…”