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Structural variability, coordination and adaptation of a native photosynthetic machinery

Nature Plants volume 6, pages 869–882 (2020)Cite this article

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Abstract

Cyanobacterial thylakoid membranes represent the active sites for both photosynthetic and respiratory electron transport. We used high-resolution atomic force microscopy to visualize the native organization and interactions of photosynthetic complexes within the thylakoid membranes from the model cyanobacterium Synechococcus elongatus PCC 7942. The thylakoid membranes are heterogeneous and assemble photosynthetic complexes into functional domains to enhance their coordination and regulation. Under high light, the chlorophyll-binding proteins IsiA are strongly expressed and associate with Photosystem I (PSI), forming highly variable IsiA−PSI supercomplexes to increase the absorption cross-section of PSI. There are also tight interactions of PSI with Photosystem II (PSII), cytochrome b6f, ATP synthase and NAD(P)H dehydrogenase complexes. The organizational variability of these photosynthetic supercomplexes permits efficient linear and cyclic electron transport as well as bioenergetic regulation. Understanding the organizational landscape and environmental adaptation of cyanobacterial thylakoid membranes may help inform strategies for engineering efficient photosynthetic systems and photo-biofactories.

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Fig. 1: AFM images of native thylakoid membranes from ML- and HL-adapted Syn7942 cells.
Fig. 2: Removal of the cytoplasmic subunits of PSI by AFM nanodissection.
Fig. 3: AFM topographs of thylakoid membranes from HL-adapted Syn7942 cells.
Fig. 4: Analysis of IsiA organization.
Fig. 5: Functional characterization of IsiA in Syn7942 cells under ML, HL and Fe–conditions.
Fig. 6: AFM images reveal PSII and Cyt b6f in thylakoid membranes from ML-adapted Syn7942.
Fig. 7: AFM images of putative ATPases in thylakoid membranes.
Fig. 8: AFM images of putative NDH-1 in thylakoid membranes.

Data availability

The source data underlying Figs. 1c, 2e,f, 4a–d, 5, 6c,d,h, 7d and 8c,g, Supplementary Figs. 1b,c, 2a–c, 4b,d, 9b,d, 12b and 14b and Supplementary Tables 1 and 2 are provided as a Source Data file. All data are available from the corresponding author upon request.

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Acknowledgements

We thank J. Rodriguez-Ramos for support with AFM data analysis and F. Zhao for data analysis. We thank the Liverpool Centre for Cell Imaging and Centre for Proteome Research for technical assistance and provision in AFM imaging, mass spectroscopy and data analysis. We also thank G. F. Dykes and A. Beckett for technical support with EM. This work was supported by the Royal Society University Research Fellowship (nos. UF120411 and URF\R\180030 to L.-N.L.), Royal Society grants (nos. RGF\EA\181061, RGF\EA\180233 and IEC\NSFC\191600 to L.-N.L.), Biotechnology and Biological Sciences Research Council grants (nos. BB/R003890/1, BB/M024202/1, BB/M012441/1 to L.-N.L.), the Queen Mary Principal’s research studentship (to S.W.), the National Science Foundation of China (nos. 31630012, U1706207 and 91851205 to Y.-Z.Z.), the National Key R&D Program of China (no. 2018YFC1406700 to Y.-Z.Z.), the Major Scientific and Technological Innovation Project of Shandong Province (no. 2019JZZY010817 to Y.-Z.Z.), the AoShan Talents Cultivation Program supported by the Pilot National Laboratory for Marine Science and Technology (Qingdao), China (no. 2017ASTCP-OS14 to Y.-Z.Z.), the Taishan Scholars Program of Shandong Province, China (no. tspd20181203 to Y.-Z.Z.), the National Natural Science Foundation of China (nos. 31770128 and 91851103 to Q.W.) and the China Postdoctoral Science Foundation Funded Project (no. 2019M662335 to L.-S.Z.).

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Authors and Affiliations

  1. State Key Laboratory of Microbial Technology, and Marine Biotechnology Research Center, Shandong University, Qingdao, China

    Long-Sheng Zhao & Yu-Zhong Zhang

  2. Institute of Integrative Biology, University of Liverpool, Liverpool, UK

    Long-Sheng Zhao, Tuomas Huokko, Deborah M. Simpson & Lu-Ning Liu

  3. College of Marine Life Sciences and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China

    Long-Sheng Zhao, Yu-Zhong Zhang & Lu-Ning Liu

  4. Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, China

    Long-Sheng Zhao & Yu-Zhong Zhang

  5. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Sam Wilson, Alexander V. Ruban & Conrad W. Mullineaux

  6. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China

    Qiang Wang

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Contributions

L.-S.Z., Y.-Z.Z. and L.-N.L. conceived the project. L.-S.Z., T.H., S.W., D.M.S., C.W.M. and L.-N.L. performed the research. L.-S.Z., T.H. S.W., D.M.S., Q.W., A.V.R., C.W.M., Y.-Z.Z. and L.-N.L. analysed the data. L.-S.Z., T.H., C.W.M., Y.-Z.Z. and L.-N.L. wrote the manuscript. All authors discussed and commented on the results and the manuscript.

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Correspondence to Yu-Zhong Zhang or Lu-Ning Liu.

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Supplementary Tables 1–3, Figs. 1–18 and references.

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Supplementary Data File 1

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Supplementary Data File 3

Unprocessed immunoblots and gels corresponding to the immunoblots and gels presented in Supplementary Fig. 2.

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Statistical source data for Supplementary Fig. 9.

Supplementary Data File 6

Unprocessed immunoblots and gels corresponding to the immunoblots and gels presented in Supplementary Fig. 9.

Supplementary Data File 7

Statistical source data for Supplementary Fig. 12.

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Supplementary Data File 9

Statistical source data for Supplementary Table 1.

Supplementary Data File 10

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Zhao, LS., Huokko, T., Wilson, S. et al. Structural variability, coordination and adaptation of a native photosynthetic machinery. Nat. Plants 6, 869–882 (2020). https://doi.org/10.1038/s41477-020-0694-3

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