Structures and organizations of PSI-AcpPCI supercomplexes from red tidal and coral symbiotic photosynthetic dinoflagellates

Abstract

Marine photosynthetic dinoflagellates are a group of successful phytoplankton that can form red tides in the ocean and also symbiosis with corals. These features are closely related to the photosynthetic properties of dinoflagellates. We report here three structures of photosystem I (PSI)-chlorophylls (Chls) a/c-peridinin protein complex (PSI-AcpPCI) from two species of dinoflagellates by single-particle cryoelectron microscopy. The crucial PsaA/B subunits of a red tidal dinoflagellate Amphidinium carterae are remarkably smaller and hence losing over 20 pigment-binding sites, whereas its PsaD/F/I/J/L/M/R subunits are larger and coordinate some additional pigment sites compared to other eukaryotic photosynthetic organisms, which may compensate for the smaller PsaA/B subunits. Similar modifications are observed in a coral symbiotic dinoflagellate Symbiodinium species, where two additional core proteins and fewer AcpPCIs are identified in the PSI-AcpPCI supercomplex. The antenna proteins AcpPCIs in dinoflagellates developed some loops and pigment sites as a result to accommodate the changed PSI core, therefore the structures of PSI-AcpPCI supercomplex of dinoflagellates reveal an unusual protein assembly pattern. A huge pigment network comprising Chls a and c and various carotenoids is revealed from the structural analysis, which provides the basis for our deeper understanding of the energy transfer and dissipation within the PSI-AcpPCI supercomplex, as well as the evolution of photosynthetic organisms.

Keywords: cryoelectron microscopy; dinoflagellates; light-harvesting antennae; photosynthesis; photosystem I.

Fig. 1.

Overall structures of PSI-AcpPCI supercomplex from A. carterae (Left) and Symbiodinium (Right). (A) Top view of Ac-PSI–AcpPCI supercomplex from the stromal side. (B) Side view of Ac-PSI–AcpPCI supercomplex. (C) Two AcpPCI antennae layers surrounding the PSI core in Ac-PSI–AcpPCI supercomplex. (D-F) Detailed subunits of Ss-PSI–AcpPCI supercomplex from the top and side views. In (A), (B), (D), and (E), protein subunits are shown as cylindrical cartoons and colored individually as indicated. In (C) and (F), AcpPCIs in the inner layer and the outer layer are indicated by red and blue cartoons, respectively.

Fig. 2.

Comparisons of the PSI core subunit structures between A. carterae and C. gracilis. (A) Conserved secondary structures of Ac-PSI core (gray) and the additional subunits of PsaD/F/I/J/L/M/R. (B) Different loop structures of PsaA/B between A. carterae (light pink/green) and C. gracilis (gray) at the stromal (Left) and lumenal (Right) sides, respectively. The 11 transmembrane helices of PsaA/B are labeled with red numbers, and the loop regions with significant structural differences between A. carterae and C. gracilis are labeled with red asterisks. (C) Comparisons of the Chl and Car sites in the PsaA/B. (D) Comparisons of the PsaD/F/I/J/L/M/R structures between A. carterae (colorful) and C. gracilis (gray). Conserved pigment sites are shown in sticks with the same colors as their subunits, whereas specific pigment-binding sites in A. carterae and C. gracilis PSI are indicated by green bold and cyan bold sticks, respectively.

Fig. 3.

Assembly and interactions of Ac-PSI core subunits. Four regions of interactions mediated mainly by PsaD (A), PsaR (B), PsaL (C), and PsaF/M (D) shown in cartoons. The color codes of subunits are the same as those in Fig. 1.

Fig. 4.

The structures, locations, and phylogenetic analysis of Ac-AcpPCI antennae. (A) The pigment sites, secondary structures, and locations of five representative Ac-AcpPCIs (Ac-AcpPCI-1/3/4/7/8/15) around the Ac-PSI core. The Chl a, Chl c, Per, Ddx, and Din molecules are shown in green, blue, medium purple, gold, and coral sticks, respectively. (B) Phylogenetic tree analysis of the light-harvesting antennae from A. carterae, C. merolae, C. gracilis, P. tricornutum, and T. pseudonana. The groups of Lhcr and Lhcf types are labeled in blue and green, respectively, whereas the antennae of A. carterae are labeled in red.

Fig. 5.

Pigment arrangement and proposed EET pathways in the Ac-PSI–AcpPCI supercomplex. (A) Distribution of all pigments in the Ac-PSI–AcpPCI supercomplex. Chls a in Ac-AcpPCIs, Chls a in the PSI core, Chls c, Pers, Ddxs, Dins, and Bcrs are shown in green, cyan, blue, purple, gold, light coral, and gray sticks, respectively. Coupled Chl a-a pairs are colored in red. (B) Distribution of all Cars. (C) EET within Ac-PSI–AcpPCI at the stromal side. (D) EET pathways at the lumenal side. In (C) and (D), the EET pathways from outer to inner Ac-AcpPCIs and inner Ac-AcpPCIs to the PSI core are indicated by black arrows, and the additional EET pathways from inner Ac-AcpPCIs to the PSI core are indicated by red arrows. The proposed EET pathways among Chls a in Ac-AcpPCIs are labeled by black dashed lines. All special Chls a associated with EET are indicated by bold sticks.

Fig. 6.

Possible evolutionary changes of PSI–antennae from the cyanobacteria to the green and red lineages. PDB codes of PSI structures: PSI of a cyanobacterium (Synechococcus elongatus,1JB0); PSI–LHCI of a green alga (Ostreococcus tauri, 7YCA), a moss (Physcomitrium patens, 7XQP), a higher plant (Zea mays, 5ZJI); PSI–LHCR of a red alga (C. merolae, 5ZGB); PSI–ACPI of a cryptophyte alga (Chroomonas placoidea, 7Y7B); PSI–FCPI of a diatom (C. gracilis, 6LY5); PSI–AcpPCI of a dinoflagellate (A.carterae, 8JW0). The evolutionary process of PSI–antennae from C. merolae to A. carterae is highlighted by the red dashed box. During this process, the PasA/B subunits have lost certain loop regions (indicated by the red scissor in the figure), while the PsaD/F/I/J/L/M subunits have gained extra secondary structure motifs and longer termini (the additional regions are colored, following the previous color).