Carotenoid assembly regulates quinone diffusion and the Roseiflexus castenholzii reaction center-light harvesting complex architecture

• Published in: eLife 2023-09, Vol.12
• Main Authors: Xin, Jiyu, Shi, Yang, Zhang, Xin, Yuan, Xinyi, Xin, Yueyong, He, Huimin, Shen, Jiejie, Blankenship, Robert E, Xu, Xiaoling
• Format: Article
• Language: English
• Subjects: Bacteria; Bacteriochlorophyll; carotenoid; Carotenoids; Chlorophyll; Cytochrome; Cytochrome c; Data collection; filamentous anoxygenic phototroph; Foreign exchange rates; light harvesting complex; Microscopy; Photosynthesis; Photosynthetic apparatus; Pigments; Plant Biology; Proteins; quinone exchange; Quinones; reaction center; Roseiflexus castenholzii; Structural Biology and Molecular Biophysics
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.88951

Carotenoid (Car) pigments perform central roles in photosynthesis-related light harvesting (LH), photoprotection, and assembly of functional pigment-protein complexes. However, the relationships between Car depletion in the LH, assembly of the prokaryotic reaction center (RC)-LH complex, and quinone exchange are not fully understood. Here, we analyzed native RC-LH (nRC-LH) and Car-depleted RC-LH (dRC-LH) complexes in Roseiflexus castenholzii , a chlorosome-less filamentous anoxygenic phototroph that forms the deepest branch of photosynthetic bacteria. Newly identified exterior Cars functioned with the bacteriochlorophyll B800 to block the proposed quinone channel between LHαβ subunits in the nRC-LH, forming a sealed LH ring that was disrupted by transmembrane helices from cytochrome c and subunit X to allow quinone shuttling. dRC-LH lacked subunit X, leading to an exposed LH ring with a larger opening, which together accelerated the quinone exchange rate. We also assigned amino acid sequences of subunit X and two hypothetical proteins Y and Z that functioned in forming the quinone channel and stabilizing the RC-LH interactions. This study reveals the structural basis by which Cars assembly regulates the architecture and quinone exchange of bacterial RC-LH complexes. These findings mark an important step forward in understanding the evolution and diversity of prokaryotic photosynthetic apparatus. Photosynthesis is a biological process that converts energy from sunlight into a form of chemical energy that supports almost all life on Earth. Over the course of evolution, photosynthesis has gone from being only performed by bacteria to appearing in algae and green plants. While this has given rise to a range of different machineries for photosynthesis, the process always begins the same way: with a structure called the reaction center-light harvesting (RC-LH) complex. Two pigments in the light-harvesting (LH) region – known as chlorophyll and carotenoids – absorb light energy and transfer it to another part of the complex known as the quinone-type reaction center (RC). This results in the release of electrons that interact with a molecule called quinone converting it to hydroquinone. The electron-bound hydroquinone then shuttles to other locations in the cell where it initiates further steps that ultimately synthesize forms of chemical energy that can power essential cellular processes. In photosynthetic bacteria, hydroquinone must first pass through a ring str