Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences and The Affiliated Hospital of Hangzhou Normal University, Hangzhou, China
Yang Shi
Liangzhu Laboratory, MOE Frontier Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-machine Intelligence & Department of Neurobiology and Department of Pathology of the First Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang University, Hangzhou, China
Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences and The Affiliated Hospital of Hangzhou Normal University, Hangzhou, China; Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China
Xinyi Yuan
Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences and The Affiliated Hospital of Hangzhou Normal University, Hangzhou, China; Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China
Yueyong Xin
Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China
Huimin He
Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China
Jiejie Shen
Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences and The Affiliated Hospital of Hangzhou Normal University, Hangzhou, China
Robert E Blankenship
Departments of Biology and Chemistry, Washington University in St. Louis, St. Louis, United States
Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences and The Affiliated Hospital of Hangzhou Normal University, Hangzhou, China; Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China
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.
