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. 2022 Jun 17;13(1):3389.
doi: 10.1038/s41467-022-30962-9.

Core and rod structures of a thermophilic cyanobacterial light-harvesting phycobilisome

Affiliations

Core and rod structures of a thermophilic cyanobacterial light-harvesting phycobilisome

Keisuke Kawakami et al. Nat Commun. .

Abstract

Cyanobacteria, glaucophytes, and rhodophytes utilize giant, light-harvesting phycobilisomes (PBSs) for capturing solar energy and conveying it to photosynthetic reaction centers. PBSs are compositionally and structurally diverse, and exceedingly complex, all of which pose a challenge for a comprehensive understanding of their function. To date, three detailed architectures of PBSs by cryo-electron microscopy (cryo-EM) have been described: a hemiellipsoidal type, a block-type from rhodophytes, and a cyanobacterial hemidiscoidal-type. Here, we report cryo-EM structures of a pentacylindrical allophycocyanin core and phycocyanin-containing rod of a thermophilic cyanobacterial hemidiscoidal PBS. The structures define the spatial arrangement of protein subunits and chromophores, crucial for deciphering the energy transfer mechanism. They reveal how the pentacylindrical core is formed, identify key interactions between linker proteins and the bilin chromophores, and indicate pathways for unidirectional energy transfer.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Overall structure of the PBS core from T. vulcanus.
Cryo-EM map of the PBS core from the front (a, c), side (b, e, f), and bottom (d) views. c It shows the superposition of the cryo-EM map and the refined PBS core model. e Here it shows the structure inside the rectangle in a, enlarged and rotated 90 ̊. f This shows e rotated 180 ̊. g Schematic model of the pentacylindrical APC core (including A (A’), B, and C (C’) cylinders) and PC rods (Rb, Rb’, Rt, and Rt’). ApcE (LCM) containing α, Reps 1–4 and Arms 1–3 is shown in red. PC rods that did not build the model are shown in translucent. The PC rod models were drawn referencing the cryo-EM map in this study and the PBS structure from Nostoc 7120. h Schematic model of the PC rod. CpcC (LR), CpcD (LRT), and CpcG (LRC) interact within the two PC hexamers. The identification of ApcD is tentative. ApcD is shown in parentheses (ApcD).
Fig. 2
Fig. 2. Structures of A, B, and C cylinders, including terminal emitters and linker proteins.
a Arrangement of the terminal emitters (αLCM of ApcE [LCM] and ApcD), ApcF, and linker proteins (ApcE [LCM] and ApcCs). b Structures of APC trimer (A3) and Rep1 of ApcE (LCM) in A cylinder. c Structures of APC trimers A1 and A2, ApcC, and Rep2 of ApcE (LCM) in A cylinder. d Structures of APC trimers B1 and B2, ApcC, Rep3, and Arm3 of ApcE (LCM) in B cylinder. e Structure of APC trimers C1 and C2, ApcC, and Rep4 of ApcE (LCM) in C’ cylinder. f Superposition of four Rep structures (Reps1–4). Dashed lines indicate the α-helixes in the Rep regions. Rep1, green; Rep2, red; Rep3, blue; Rep4, cyan.
Fig. 3
Fig. 3. Arrangement of chromophores is the key to the energy transfer pathway in PBS core.
a Possible energy transfer pathways in and between B and C (C’) cylinders. b Possible energy transfer pathways in and between A and C cylinders. c Possible energy transfer pathways between A (A’) and B cylinders. d–g The chromophores and the surrounding amino acid residues of ApcE (LCM). The numbers near the dotted lines indicate the distances (Å) between the PCB pairs. In e–g, dashed lines (black and green) indicate hydrogen bonds, and dotted lines (blue) indicate covalent bonds between PCB and cysteine residue. In the amino acid residues (Phe992/ApcE and Cys84/C1) in d, the directions of atoms from Cα to Cβ in the residues are indicated by the capsule-shaped objects. The identification of ApcD is tentative, and the chromophore in ApcD (A1αApcD81) is indicated in parentheses.
Fig. 4
Fig. 4. Chromophores and their surrounding structures in terminal emitter (ApcE [LCM]) and ApcF.
a, b Chromophores in the APC trimer A3 and their interaction with Rep1 of ApcE. c Chromophore in the APC trimer A2 and its interaction with Rep2 of ApcE. d Chromophore of ApcF and its interaction with Rep1 of ApcE. e Chromophore of ApcE and its interaction with ApcF. The dashed lines (black) indicate hydrogen bonds. The dotted lines (blue) indicate covalent bonds between PCB and cysteine residue. Amino acid residues for which the side-chain arrangement cannot be precisely displayed are indicated with capsule-shaped objects. The directions of atoms from Cα to Cβ in the residues are indicated by the capsule-shaped objects.
Fig. 5
Fig. 5. Comparison of chromophores and their surrounding structures in the terminal emitters (ApcE [LCM]) of each species.
a Crystal structure of Nostoc 7120 ApcE at 2.2 Å resolution. b Cryo-EM structure of the red algal P. purpureum ApcE at 2.8 Å resolution. c Cryo-EM structure of the red algal G. pacifica ApcE at 3.5 Å resolution. d Cryo-EM structure of the cyanobacterial Synechococcus 7002 ApcE at 3.5 Å resolution. e Cryo-EM structure of the cyanobacterial Nostoc ApcE at 3.9 Å resolution. f Cryo-EM structure of the cyanobacterial T. vulcanus ApcE at 3.7 Å resolution. These ApcE structures were superimposed with their density map contoured at 1σ (a), 3σ (b), 2σ (c), 5σ (d), 3σ (e), and 3σ (f). Amino acid residues for which the side-chain arrangement cannot be precisely displayed are indicated with capsule-shaped objects. The directions of atoms from Cα to Cβ in the residues are indicated by the capsule-shaped objects.
Fig. 6
Fig. 6. Structure of PC rod including linker protein.
a cryo-EM map of the PC rod (Disk A and Disk B). b Arrangement of the linker proteins (CpcC, CpcD, and CpcG) in the PC rod. c Structure of the PC rod in b rotated 90 ̊.
Fig. 7
Fig. 7. Structural comparison of PC rods solved by cryo-EM (PDB: 7VEB) and X-ray crystallography (PDB: 3O2C).
a Superimposition of the top parts of Disk A. The linker protein CpcD (residues 55–65 [red in "panel 1"] and 68–74 [green in "panel 1"]) interacts with a CpcB region (residues 109–122 [orange in "panel 1"]) in PC monomer 3. b Superposition of the lower parts of Disk A. The linker protein CpcC (residues 123–127 [cyan in "panel 2"] and 197–204 [green in "panel 3"]) interacts with CpcB regions (residues 14–17 [green in "panel 2"] of PC monomer 5 and 113–122 [cyan in "panel 3"] of PC monomer 6, respectively). c Superimposition of the top parts of Disk B. The "CpcD-like structure (residues 234–287)" in CpcC interacts with a CpcB region (residues 109–122, orange in "panel 4") in PC monomer 9. The RMSD of the regions (residues 234–287) in CpcC and CpcD is 1.3. d Superposition of the lower parts of Disk B. The linker protein CpcG2 (residues 9–38 [green in "panel 5"]) interacts with regions in monomers 10 (residues 78–90 and 109–122 [yellow in "panel 5"]) and 11 (residues 1–15 and 105–115 [yellow in "panel 5"]). The areas marked "1–5" are the magnified view of the interacting parts of the linker proteins and each PC monomer. Helix and transparent surface models represent PC rods solved by cryo-EM and X-ray crystallography, respectively. Panels 1–6 show magnified views of the interactions of each PC trimer with the linker proteins.
Fig. 8
Fig. 8. Possible energy transfer pathway in the PC rod.
a Arrangement of chromophores in the PC rod. α84, β84, and β155 are colored cyan, green, and yellow, respectively. b Arrangement of β84s in a PC rod interacting with linker proteins. β84s at the boundary between Disk A and Disk B are colored green, and these chromophores are involved in the energy transfer between Disk A and Disk B. The amino acid residues of the linker proteins near β84s are indicated in B.

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