A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph

Abstract Halorhodospira (Hlr.) halophila strain BN9622 is an extremely halophilic and alkaliphilic phototrophic purple sulfur bacterium isolated from a hypersaline lake in the Libyan Desert whose total salinity exceeded 35% at pH 10.7. Here we present a cryo-EM structure of the native LH1–LH2 co-com...

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Main Authors: Kazutoshi Tani, Kenji V. P. Nagashima, Risa Kojima, Masaharu Kondo, Ryo Kanno, Issei Satoh, Mai Kawakami, Naho Hiwatashi, Kazuna Nakata, Sakiko Nagashima, Kazuhito Inoue, Yugo Isawa, Ryoga Morishita, Shinichi Takaichi, Endang R. Purba, Malgorzata Hall, Long-Jiang Yu, Michael T. Madigan, Akira Mizoguchi, Bruno M. Humbel, Yukihiro Kimura, Yutaka Nagasawa, Takehisa Dewa, Zheng-Yu Wang-Otomo
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55811-9
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author Kazutoshi Tani
Kenji V. P. Nagashima
Risa Kojima
Masaharu Kondo
Ryo Kanno
Issei Satoh
Mai Kawakami
Naho Hiwatashi
Kazuna Nakata
Sakiko Nagashima
Kazuhito Inoue
Yugo Isawa
Ryoga Morishita
Shinichi Takaichi
Endang R. Purba
Malgorzata Hall
Long-Jiang Yu
Michael T. Madigan
Akira Mizoguchi
Bruno M. Humbel
Yukihiro Kimura
Yutaka Nagasawa
Takehisa Dewa
Zheng-Yu Wang-Otomo
author_facet Kazutoshi Tani
Kenji V. P. Nagashima
Risa Kojima
Masaharu Kondo
Ryo Kanno
Issei Satoh
Mai Kawakami
Naho Hiwatashi
Kazuna Nakata
Sakiko Nagashima
Kazuhito Inoue
Yugo Isawa
Ryoga Morishita
Shinichi Takaichi
Endang R. Purba
Malgorzata Hall
Long-Jiang Yu
Michael T. Madigan
Akira Mizoguchi
Bruno M. Humbel
Yukihiro Kimura
Yutaka Nagasawa
Takehisa Dewa
Zheng-Yu Wang-Otomo
author_sort Kazutoshi Tani
collection DOAJ
description Abstract Halorhodospira (Hlr.) halophila strain BN9622 is an extremely halophilic and alkaliphilic phototrophic purple sulfur bacterium isolated from a hypersaline lake in the Libyan Desert whose total salinity exceeded 35% at pH 10.7. Here we present a cryo-EM structure of the native LH1–LH2 co-complex from strain BN9622 at 2.22 Å resolution. Surprisingly, the LH1–LH2 co-complex consists of a double-ring cylindrical structure with the larger LH1 ring encircling a smaller LH2 ring. The Hlr. halophila LH1 contains 18 αβ-subunits and additional bacteriochlorophyll a (BChl a) molecules that absorb maximally at 797 nm. The LH2 ring is composed of 9 αβ-subunits, and the BChl a molecules in the co-complex form extensive intra- and inter-complex networks to allow near 100% efficiency of energy transfer to its surrounding LH1. The additional LH1-B797 BChls a are located in such a manner that they facilitate exciton transfer from monomeric BChls in LH2 to the dimeric BChls in LH1. The structural features of the strain BN9622 LH1–LH2 co-complex may have evolved to allow a minimal LH2 complex to maximize excitation transfer to the core complex and effectively harvest light in the physiologically demanding ecological niche of this purple bacterium.
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spelling doaj-art-dcae5f45d49d4f61b819e03e9eed91282025-02-09T12:46:20ZengNature PortfolioNature Communications2041-17232025-02-0116111210.1038/s41467-024-55811-9A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototrophKazutoshi Tani0Kenji V. P. Nagashima1Risa Kojima2Masaharu Kondo3Ryo Kanno4Issei Satoh5Mai Kawakami6Naho Hiwatashi7Kazuna Nakata8Sakiko Nagashima9Kazuhito Inoue10Yugo Isawa11Ryoga Morishita12Shinichi Takaichi13Endang R. Purba14Malgorzata Hall15Long-Jiang Yu16Michael T. Madigan17Akira Mizoguchi18Bruno M. Humbel19Yukihiro Kimura20Yutaka Nagasawa21Takehisa Dewa22Zheng-Yu Wang-Otomo23Center for Computational Sciences, University of TsukubaResearch Institute for Integrated Science, Kanagawa UniversityCollege of Life Sciences, Ritsumeikan UniversityDepartment of Life Science and Applied Chemistry, Graduate School of Engineering, Nagoya Institute of TechnologyQuantum Wave Microscopy Unit, Okinawa Institute of Science and Technology Graduate University (OIST)Faculty of Science, Ibaraki UniversityFaculty of Science, Ibaraki UniversityFaculty of Science, Ibaraki UniversityDepartment of Agrobioscience, Graduate School of Agriculture, Kobe UniversityResearch Institute for Integrated Science, Kanagawa UniversityResearch Institute for Integrated Science, Kanagawa UniversityCollege of Life Sciences, Ritsumeikan UniversityDepartment of Life Science and Applied Chemistry, Graduate School of Engineering, Nagoya Institute of TechnologyDepartment of Molecular Microbiology, Faculty of Life Science, Tokyo University of AgricultureScientific Imaging Section, Okinawa Institute of Science and Technology Graduate University (OIST)Scientific Imaging Section, Okinawa Institute of Science and Technology Graduate University (OIST)Key Laboratory of Photobiology, Photosynthesis Research Center, Institute of Botany, Chinese Academy of SciencesSchool of Biological Sciences, Department of Microbiology, Southern Illinois UniversityGraduate School of Medicine, Mie UniversityProvost Office, Okinawa Institute of Science and Technology Graduate University (OIST)Department of Agrobioscience, Graduate School of Agriculture, Kobe UniversityCollege of Life Sciences, Ritsumeikan UniversityDepartment of Life Science and Applied Chemistry, Graduate School of Engineering, Nagoya Institute of TechnologyFaculty of Science, Ibaraki UniversityAbstract Halorhodospira (Hlr.) halophila strain BN9622 is an extremely halophilic and alkaliphilic phototrophic purple sulfur bacterium isolated from a hypersaline lake in the Libyan Desert whose total salinity exceeded 35% at pH 10.7. Here we present a cryo-EM structure of the native LH1–LH2 co-complex from strain BN9622 at 2.22 Å resolution. Surprisingly, the LH1–LH2 co-complex consists of a double-ring cylindrical structure with the larger LH1 ring encircling a smaller LH2 ring. The Hlr. halophila LH1 contains 18 αβ-subunits and additional bacteriochlorophyll a (BChl a) molecules that absorb maximally at 797 nm. The LH2 ring is composed of 9 αβ-subunits, and the BChl a molecules in the co-complex form extensive intra- and inter-complex networks to allow near 100% efficiency of energy transfer to its surrounding LH1. The additional LH1-B797 BChls a are located in such a manner that they facilitate exciton transfer from monomeric BChls in LH2 to the dimeric BChls in LH1. The structural features of the strain BN9622 LH1–LH2 co-complex may have evolved to allow a minimal LH2 complex to maximize excitation transfer to the core complex and effectively harvest light in the physiologically demanding ecological niche of this purple bacterium.https://doi.org/10.1038/s41467-024-55811-9
spellingShingle Kazutoshi Tani
Kenji V. P. Nagashima
Risa Kojima
Masaharu Kondo
Ryo Kanno
Issei Satoh
Mai Kawakami
Naho Hiwatashi
Kazuna Nakata
Sakiko Nagashima
Kazuhito Inoue
Yugo Isawa
Ryoga Morishita
Shinichi Takaichi
Endang R. Purba
Malgorzata Hall
Long-Jiang Yu
Michael T. Madigan
Akira Mizoguchi
Bruno M. Humbel
Yukihiro Kimura
Yutaka Nagasawa
Takehisa Dewa
Zheng-Yu Wang-Otomo
A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph
Nature Communications
title A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph
title_full A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph
title_fullStr A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph
title_full_unstemmed A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph
title_short A distinct double-ring LH1–LH2 photocomplex from an extremophilic phototroph
title_sort distinct double ring lh1 lh2 photocomplex from an extremophilic phototroph
url https://doi.org/10.1038/s41467-024-55811-9
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