Structure of a dimeric photosystem II complex from a cyanobacterium acclimated to far-red light

• Published in: The Journal of biological chemistry 2023-01, Vol.299 (1), p.102815, Article 102815
• Main Authors: Gisriel, Christopher J., Shen, Gaozhong, Flesher, David A., Kurashov, Vasily, Golbeck, John H., Brudvig, Gary W., Amin, Muhamed, Bryant, Donald A.
• Format: Article
• Language: English
• Subjects: Acclimatization; BASIC BIOLOGICAL SCIENCES; chlorophyll; Chlorophyll - metabolism; Chlorophyll A - metabolism; cofactor assignment; cryo-EM; cyanobacteria; Cyanobacteria - metabolism; Cyanobacteria - physiology; electron transfer; energy transfer; far-red light photoacclimation; INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Light; Photosynthesis; Photosystem I Protein Complex - metabolism; photosystem II; Photosystem II Protein Complex - chemistry; Protein Multimerization; PsbH
• ISSN: 0021-9258; 1083-351X; 1083-351X
• DOI: 10.1016/j.jbc.2022.102815

Photosystem II (PSII) is the water-splitting enzyme central to oxygenic photosynthesis. To drive water oxidation, light is harvested by accessory pigments, mostly chlorophyll (Chl) a molecules, which absorb visible light (400–700 nm). Some cyanobacteria facultatively acclimate to shaded environments by altering their photosynthetic machinery to additionally absorb far-red light (FRL, 700–800 nm), a process termed far-red light photoacclimation or FaRLiP. During far-red light photoacclimation, FRL-PSII is assembled with FRL-specific isoforms of the subunits PsbA, PsbB, PsbC, PsbD, and PsbH, and some Chl-binding sites contain Chls d or f instead of the usual Chl a. The structure of an apo-FRL-PSII monomer lacking the FRL-specific PsbH subunit has previously been determined, but visualization of the dimeric complex has remained elusive. Here, we report the cryo-EM structure of a dimeric FRL–PSII complex. The site assignments for Chls d and f are consistent with those assigned in the previous apo-FRL-PSII monomeric structure. All sites that bind Chl d or Chl f at high occupancy exhibit a FRL-specific interaction of the formyl moiety of the Chl d or Chl f with the protein environment, which in some cases involves a phenylalanine sidechain. The structure retains the FRL-specific PsbH2 subunit, which appears to alter the energetic landscape of FRL-PSII, redirecting energy transfer from the phycobiliprotein complex to a Chl f molecule bound by PsbB2 that acts as a bridge for energy transfer to the electron transfer chain. Collectively, these observations extend our previous understanding of the structure-function relationship that allows PSII to function using lower energy FRL.