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Structure of photosynthetic LH1–RC supercomplex at 1.9 Å resolution

Nature volume 556, pages 209–213 (2018)Cite this article

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Abstract

Light-harvesting complex 1 (LH1) and the reaction centre (RC) form a membrane-protein supercomplex that performs the primary reactions of photosynthesis in purple photosynthetic bacteria. The structure of the LH1–RC complex can provide information on the arrangement of protein subunits and cofactors; however, so far it has been resolved only at a relatively low resolution. Here we report the crystal structure of the calcium-ion-bound LH1–RC supercomplex of Thermochromatium tepidum at a resolution of 1.9 Å. This atomic-resolution structure revealed several new features about the organization of protein subunits and cofactors. We describe the loop regions of RC in their intact states, the interaction of these loop regions with the LH1 subunits, the exchange route for the bound quinone QB with free quinone molecules, the transport of free quinones between the inside and outside of the LH1 ring structure, and the detailed calcium-ion-binding environment. This structure provides a solid basis for the detailed examination of the light reactions that occur during bacterial photosynthesis.

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Fig. 1: Architecture of LH1–RC from Tch. tepidum at a resolution of 1.9 Å.
Fig. 2: Differences between the isolated and intact RC core structures.
Fig. 3: Distribution of quinones and lipids in LH1–RC.
Fig. 4: Interactions between LH1 and RC, and among LH1.
Fig. 5: Calcium-binding sites in LH1.

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Acknowledgements

We thank M. T. Madigan for providing the Tch. tepidum strain MC; F. Ma, Y. Xin, Y. Umena, X. Chen, X. Qin, W. Wang and T. Kawakami for discussion and assistance during the experiments and data analysis. This work was supported by JSPS KAKENHI No. JP24000018 and JP17H0643419 (to J.-R.S.), JP16H04174 (to Z.-Y.W.-O.), JP16H06296 and JP16H06162 (to M.S.), a program for promoting the enhancement of research universities at Okayama University from MEXT, Japan, and performed using the beamlines BL41XU (proposal numbers 2014B1277, 2015A1079, 2015B2079, 2016A2553, 2017A2590 to L.-J.Y.) and BL44XU (2015B6522, 2016A6621, 2016B6621, 2017A6724, 2017B6724 to M.S.) at SPring-8, and BL-1A at Photon Factory, Japan (2016R-27 to L.-J.Y.). We thank staff members of SPring-8 and Photon Factory for their assistance with data collection.

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Nature thanks R. Cogdell and R. Niederman for their contribution to the peer review of this work.

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Authors and Affiliations

  1. Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University, Okayama, Japan

    Long-Jiang Yu, Michihiro Suga & Jian-Ren Shen

  2. Faculty of Science, Ibaraki University, Mito, Japan

    Zheng-Yu Wang-Otomo

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Contributions

J.-R.S. and L.-J.Y. conceived the project; L.-J.Y. prepared the samples with the help of Z.-Y.W.-O.; L.-J.Y. grew the crystals under the supervision of J.-R.S.; L.-J.Y. and M.S. collected the diffraction data and analysed the structure; L.-J.Y. and J.-R.S. wrote the manuscript; and all authors contributed to the discussion and improvement of the manuscript.

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Correspondence to Jian-Ren Shen.

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Extended data figures and tables

Extended Data Fig. 1 Quality of the LH1–RC crystal and its packing pattern.

a, An image of the LH1–RC crystals obtained in the present study. These crystals were obtained reproducibly under the present crystallization conditions. b, A typical diffraction image of the LH1–RC crystal taken at BL41XU of SPring-8, Japan, with a wavelength of 1.0 Å at 100 K. This diffraction image was obtained reproducibly with many crystals tested. c, d, Packing patterns of the previous (c) and the present crystal (d).

Extended Data Fig. 2 Close-up views of the electron density maps for some of the cofactors of LH1–RC.

The blue mesh represents the 2Fo−Fc map contoured at 1.0σ, taken at a wavelength of 1.0 Å and analysed to 1.9 Å resolution. a–d, The special-pair BChls (a), one pair of the LH1 BChls (b), one of the CDL (c) and the QB molecule (d).

Extended Data Fig. 3 Comparison of the arrangement of the cofactors between the previous and present structures.

a, Arrangement of the cofactors in the previous 3.0 Å structure, with a view from the top of the membrane. b, Superposition of the cofactors between the previous 3.0 Å and present 1.9 Å structures. c, The same as b, viewing from the side of the membrane. In b and c, the cofactors revealed in the present 1.9 Å structures are coloured differently, whereas those in the previous 3.0 Å structures are depicted in grey.

Extended Data Fig. 4 Comparison of the protein structures between the previous and present structures.

a, Superposition of the RC subunits between the previous 2.2 Å and the present 1.9 Å structures, with a side view from the membrane plane. b, Superposition of the RC subunits between the previous 3.0 Å and the present 1.9 Å structures, with a side view from the membrane plane. c, d, Superposition of the LH1 subunits between the previous 3.0 Å and present 1.9 Å structures, with a side view (c) and top view (d) relative to the membrane plane, respectively. In all panels, the present 1.9 Å structure is coloured, whereas the previous structures are depicted in grey.

Extended Data Fig. 5 Hydrogen-bonding networks for the protonation of QB.

a, Two possible proton channels connecting QB to the cytoplasmic surface. The thick arrow (coloured in blue) indicates the main channel formed within the H-subunit, which is enlarged in b, and the thin arrow indicates the second channel. b, The main hydrogen-bonding network indicated by the thick arrow in a, formed by a number of water molecules and the residues (green) from the H-subunit (pale cyan). QA and QB are depicted in violet and red, respectively, and the non-haem iron is depicted in deep purple. The hydrogen bonds are depicted as dashed lines. Water molecules participating in the hydrogen-bonding networks are depicted in orange, and those not participating are depicted in grey.

Extended Data Figure 6 Protein–protein interactions between LH1 and RC.

a–c, Interactions between the LH1 α-subunits and the RC subunits at the periplasmic side. Panels a–c correspond to boxed areas 1–3 in Fig. 4. d–f, Interactions between the LH1 α-subunits and RC subunits at the cytoplasmic side. Panels d–f correspond to boxed areas 4–6 in Fig. 4.

Extended Data Table 1 Data collection and refinement statistics
Full size table
Extended Data Table 2 Components of LH1–RC determined at 1.9 Å resolution
Full size table
Extended Data Table 3 Average B-factors of the RC subunits and the α- and β-apoproteins of LH1
Full size table
Extended Data Table 4 Interactions between LH1 and RC
Full size table

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Yu, LJ., Suga, M., Wang-Otomo, ZY. et al. Structure of photosynthetic LH1–RC supercomplex at 1.9 Å resolution. Nature 556, 209–213 (2018). https://doi.org/10.1038/s41586-018-0002-9

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