J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (10): 2262-2272.DOI: 10.1111/jipb.13628  cstr: 32098.14.jipb.13628

Special Issue: Photosynthesis

• Photosynthesis and Crop Physiology • Previous Articles     Next Articles

Structural insights into the unusual core photocomplex from a triply extremophilic purple bacterium, Halorhodospira halochloris

Chen-Hui Qi1,2†, Guang-Lei Wang1,2†, Fang-Fang Wang3, Jie Wang1,2, Xiang-Ping Wang1,2, Mei-Juan Zou1, Fei Ma1, Michael T. Madigan4, Yukihiro Kimura5*, Zheng-Yu Wang-Otomo6* and Long-Jiang Yu1*   

  1. 1. Key Laboratory of Photobiology, Photosynthesis Research Center, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
    2. University of Chinese Academy of Sciences, Beijing 100049, China
    3. Zhangjiang Lab, National Facility for Protein Science in Shanghai, Shanghai Advanced Research Institute, Chinese Academy of Sciences, Shanghai 201210, China
    4. Department of Microbiology, School of Biological Sciences, Southern Illinois University, Carbondale, IL 62901, USA
    5. Department of Agrobioscience, Graduate School of Agricultural Science, Kobe University, Nada, Kobe 657‐8501, Japan
    6. Faculty of Science, Ibaraki University, Mito 310‐8512, Japan
    These authors contributed equally to this work.
    *Correspondences: Yukihiro Kimura (ykimura@people.kobe-u.ac.jp); Zheng‐Yu Wang‐Otomo (wang@ml.ibaraki.ac.jp); Long‐Jiang Yu (longer@ibcas.ac.cn, Dr. Yu is fully responsible for the distributions of all materials associated with this article)
  • Received:2023-11-10 Accepted:2024-02-03 Online:2024-02-28 Published:2024-10-01
  • Supported by:
    This work was supported in part by the National Key R&D Program of China (No. 2022YFC3401800), National Natural Science Foundation of China (32070264), Shandong Provincial Natural Science Foundation (ZR2019ZD48), the Strategic Priority Research Program of CAS (XDA26050402), the Science & Technology Specific Project in Agricultural High‐tech Industrial Demonstration Area of the Yellow River Delta (2022SZX12), the Innovation Center for Academicians of Hainan Province, and the Specific Research Fund of the Innovation Center for Academicians of Hainan Province (No. YSPTZX202309). M.T.M. was supported in part by NASA Cooperative Agreement 80NSSC21M0355.

Abstract: Halorhodospira (Hlr.) halochloris is a triply extremophilic phototrophic purple sulfur bacterium, as it is thermophilic, alkaliphilic, and extremely halophilic. The light-harvesting-reaction center (LH1-RC) core complex of this bacterium displays an LH1-Qy transition at 1,016 nm, which is the lowest-energy wavelength absorption among all known phototrophs. Here we report the cryo-EM structure of the LH1-RC at 2.42 Å resolution. The LH1 complex forms a tricyclic ring structure composed of 16 αβγ-polypeptides and one αβ-heterodimer around the RC. From the cryo-EM density map, two previously unrecognized integral membrane proteins, referred to as protein G and protein Q, were identified. Both of these proteins are single transmembrane-spanning helices located between the LH1 ring and the RC L- subunit and are absent from the LH1-RC complexes of all other purple bacteria of which the structures have been determined so far. Besides bacteriochlorophyll b molecules (B1020) located on the periplasmic side of the Hlr. halochloris membrane, there are also two arrays of bacteriochlorophyll b molecules (B800 and B820) located on the cytoplasmic side. Only a single copy of a carotenoid (lycopene) was resolved in the Hlr. halochloris LH1-α3β3 and this was positioned within the complex. The potential quinone channel should be the space between the LH1-α3β3 that accommodates the single lycopene but does not contain a γ-polypeptide, B800 and B820. Our results provide a structural explanation for the unusual Qy red shift and carotenoid absorption in the Hlr. halochloris spectrum and reveal new insights into photosynthetic mechanisms employed by a species that thrives under the harshest conditions of any phototrophic microorganism known.

Key words: cryo-EM, LH1–RC, single carotenoid, three bacteriochlorophyll b molecules, triply extremophilic purple bacterium, unusual Qy red shift

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