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Structure of a C2S2M2N2-type PSII-LHCII supercomplex from the green alga Chlamydomonas reinhardtii - PubMed

  • ️Tue Jan 01 2019

Structure of a C2S2M2N2-type PSII-LHCII supercomplex from the green alga Chlamydomonas reinhardtii

Liangliang Shen et al. Proc Natl Acad Sci U S A. 2019.

Abstract

Photosystem II (PSII) in the thylakoid membranes of plants, algae, and cyanobacteria catalyzes light-induced oxidation of water by which light energy is converted to chemical energy and molecular oxygen is produced. In higher plants and most eukaryotic algae, the PSII core is surrounded by variable numbers of light-harvesting antenna complex II (LHCII), forming a PSII-LHCII supercomplex. In order to harvest energy efficiently at low-light-intensity conditions under water, a complete PSII-LHCII supercomplex (C2S2M2N2) of the green alga Chlamydomonas reinhardtii (Cr) contains more antenna subunits and pigments than the dominant PSII-LHCII supercomplex (C2S2M2) of plants. The detailed structure and energy transfer pathway of the Cr-PSII-LHCII remain unknown. Here we report a cryoelectron microscopy structure of a complete, C2S2M2N2-type PSII-LHCII supercomplex from C. reinhardtii at 3.37-Å resolution. The results show that the Cr-C2S2M2N2 supercomplex is organized as a dimer, with 3 LHCII trimers, 1 CP26, and 1 CP29 peripheral antenna subunits surrounding each PSII core. The N-LHCII trimer partially occupies the position of CP24, which is present in the higher-plant PSII-LHCII but absent in the green alga. The M trimer is rotated relative to the corresponding M trimer in plant PSII-LHCII. In addition, some unique features were found in the green algal PSII core. The arrangement of a huge number of pigments allowed us to deduce possible energy transfer pathways from the peripheral antennae to the PSII core.

Keywords: cryoelectron microscopy; light-harvesting complex; photosynthesis; photosystem II; structural analysis.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.

Overall architecture of the C2S2M2N2-type PSII–LHCII supercomplex from C. reinhardtii. (A) Cartoon representation of the overall structure with a top view from the stromal side. Four core subunits (D1, D2, CP43, and CP47), 1 extrinsic subunit PsbO, and the peripheral antennae are colored differently, whereas the 13 small intrinsic subunits are shown as a gray transparent surface. (B) Side view along the membrane plane. (C) The arrangement of 13 small membrane-intrinsic proteins in each monomer of the C2S2M2N2-type PSII–LHCII supercomplex viewed from the stromal side.

Fig. 2.
Fig. 2.

Structural comparison of peripheral antennae between C. reinhardtii and pea. (A) Superposition of the cryo-EM structure of the CP26 apo-protein from C. reinhardtii with that from pea (PDB ID code 5XNL). The 2 extra loop regions in Cr-CP26 are highlighted with black boxes. (B) Superposition of the cryo-EM structure of CP29 (including pigments) from C. reinhardtii with that from pea (PDB ID code 5XNL). The missing helix in Cr-CP29 is highlighted with a black box. Chl a614 existing in pea CP29 is absent in Cr-CP29. (C) Superposition of the cryo-EM structure of an LHCII subunit from the S-LHCII trimer from C. reinhardtii with that from pea (PDB ID code 5XNL). Green, C. reinhardtii; red, pea.

Fig. 3.
Fig. 3.

Sequence alignment of LHCBM subunits and the assignment of protein subunits in the cryo-EM structure from C. reinhardtii. (A) Sequence alignment of LHCBM1, LHCBM3, LHCBM6, and LHCBM7, which were detected by mass spectrometry from the SDS/PAGE bands of the Cr-PSII–LHCII supercomplex. Information on secondary structures shown above the sequences is taken from the cryo-EM structure of LHCII of the Cr-PSII–LHCII supercomplex obtained here. Helices are represented by green cylinders. Loops are denoted by dashed lines. (B–D) Assignment of the monomer 1 subunit of S-LHCII by comparison of the structural features between amino acids Thr98 and Phe98 (B), Pro133 and Glu133 (C), and Val147 and Phe147 (D). The possibilities of LHCBM1 and LHCBM7 as S-LHCII (monomer 1) in the cryo-EM structure of Cr-PSII–LHCII are excluded on the basis of B–D. (E–G) Assignment of subunit S-LHCII (monomer 3) by comparison of the structural features between amino acids Thr98 and Phe98 (E), Pro133 and Glu133 (F), and Val147 and Phe147 (G). The possibilities of LHCBM1 and LHCBM7 as S-LHCII (monomer 3) in the cryo-EM structure of Cr-PSII–LHCII are excluded on the basis of E, F and G. Thus, either LHCBM3 or LHCBM6 can be assigned to S-LHCII (monomer 1) or S-LHCII (monomer 3).

Fig. 4.
Fig. 4.

Comparison of the orientations of M-LHCII in PSII–LHCII from green algae (C. reinhardtii; green; Right) and a higher plant (pea; red; Left). For simplicity, only the peripheral antenna complexes are shown. M-LHCII is encircled with dashed lines.

Fig. 5.
Fig. 5.

Antenna–antenna and antenna–core interactions in the C2S2M2N2-type PSII–LHCII supercomplex of C. reinhardtii. (A) Surface and cartoon representations of the local structure including LHCII (S-LHCII, M-LHCII, and N-LHCII), CP26, CP29, D1, D2, CP43, CP47, PsbH, PsbI, PsbX, PsbW, and PsbZ, viewed from the stromal side. (B) Interactions between S′-LHCII (monomer 1) and CP26′. The closed interactions between S′-LHCII (monomer 1) and the extra stromal as well as luminal loops of CP26′ are highlighted with solid boxes. (C) Interactions between N-LHCII (monomer 3) and D2 mediated by PsbX. (D) Interactions between N-LHCII (monomer 1) and CP47. (E) Interactions between M-LHCII (monomer 3) and CP29. (F) Interactions between N-LHCII (monomer 1) and CP29.

Fig. 6.
Fig. 6.

Pigment arrangement and possible excitation energy transfer pathways from peripheral antenna complexes to the reaction center in the C2S2M2N2-type PSII–LHCII supercomplex of C. reinhardtii. (A) Chlorophyll distribution and possible energy transfer pathways within the whole PSII–LHCII supercomplex. Chlorophylls distributed in the stromal side layer are shown (Left), as are those distributed in the luminal side layer (Right). Chl a and Chl b are colored in green and violet, respectively. Possible energy transfer pathways from the peripheral antennae to the PSII core and among the antennae are indicated by red arrows. (B–G) The interfacial chlorophylls between M-LHCII (monomer 3) and S′-LHCII (monomer 2) (B), N-LHCII (monomer 1) and M-LHCII (monomer 3) (C), N-LHCII (monomer 1) and M-LHCII (monomer 2) (D), M-LHCII (monomer 3) and CP29 (E), N-LHCII (monomer 1) and CP29 (F), and N-LHCII (monomer 1) and CP47 (G). These panels are viewed from the side of the membrane, with the upper layer representing the stromal layer and the lower layer representing the luminal layer. Chlorophylls involved in the possible energy transfer are highlighted as sticks and labeled with blue. The Mg-to-Mg distances (Å) between 2 adjacent interfacial chlorophylls are indicated in black.

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