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Structural basis for energy and electron transfer of the photosystem I–IsiA–flavodoxin supercomplex

Nature Plants volume 6, pages 167–176 (2020)Cite this article

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Abstract

Under iron-deficiency stress, which occurs frequently in natural aquatic environments, cyanobacteria reduce the amount of iron-enriched proteins, including photosystem I (PSI) and ferredoxin (Fd), and upregulate the expression of iron-stress-induced proteins A and B (IsiA and flavodoxin (Fld)). Multiple IsiAs function as the peripheral antennae that encircle the PSI core, whereas Fld replaces Fd as the electron receptor of PSI. Here, we report the structures of the PSI3–IsiA18–Fld3 and PSI3–IsiA18 supercomplexes from Synechococcus sp. PCC 7942, revealing features that are different from the previously reported PSI structures, and a sophisticated pigment network that involves previously unobserved pigment molecules. Spectroscopic results demonstrated that IsiAs are efficient light harvesters for PSI. Three Flds bind symmetrically to the trimeric PSI core—we reveal the detailed interaction and the electron transport path between PSI and Fld. Our results provide a structural basis for understanding the mechanisms of light harvesting, energy transfer and electron transport of cyanobacterial PSI under stressed conditions.

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Fig. 1: Overall structures of the PSI3–IsiA18 and PSI3–IsiA18–Fld3 supercomplexes.
Fig. 2: Structural comparison of the PSI core part of PSI3–IsiA18 supercomplex from Synechococcus 7942, and PSI3 and PSI3–IsiA18 supercomplexes from Synechocystis 6803.
Fig. 3: The interactions between Fld and PSI.
Fig. 4: Comparison of the binding modes of Fld and Fd with the PSI core.
Fig. 5: Pigments and lipids of IsiA proteins involved in the intersubunit interactions within the PSI3–IsiA18 supercomplex.
Fig. 6: Potential excitation energy transfer pathways within the PSI3–IsiA18 supercomplex.

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Data availability

The atomic coordinates of the two supercomplexes have been deposited in the Protein Data Bank with accession codes 6KIF (for PSI3–IsiA18–Fld3) and 6KIG (for PSI3–IsiA18). The cryo-EM maps have been deposited in the Electron Microscopy Data Bank with accession codes EMD-9994 (for PSI3–IsiA18–Fld3) and EMD-9995 (for PSI3–IsiA18). The local refined maps of the two supercomplexes have been deposited along with each primary (overall) map. All other data generated or analysed are available from the corresponding authors on reasonable request.

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Acknowledgements

Cryo-EM data were collected at the Center for Biological Imaging, Core Facilities for Protein Science at the Institute of Biophysics (IBP), Chinese Academy of Sciences (CAS). We thank W. Wang and X. Lu from the Qingdao Institute of Bioenergy and Bioprocess Technology, CAS for providing the cyanobacterial strains; Y. Gong from Institute of High Energy Physics, CAS for help with protein expression; B. Zhu, X. Huang, G. Ji, D. Fan, T. Niu and F. Sun, as well as other staff members at the Center for Biological Imaging (IBP, CAS), for technical support with EM data collection; the IBP staff members Y. Chen, Z. Yang and B. Zhou for their technical support with the SPR assay; L. Niu, N. Zhu, X. Ding, M. Zhang, J. Wang and F. Yang for mass spectroscopy; J. Li and S. Liu for technical support with sample characterization; X. Zhao, H. Zhang, Y. Gao and L. Shi for the assistance in sample preparation; L. Kong for cryo-EM data storage and backup; C. Zhang from Institute of Botany, CAS for her technical support with the measurement of P700 activity; and T. Juelich from Peking University for linguistic assistance during the preparation of this manuscript. The project was funded by the National Key R&D Program of China (2017YFA0503702 and 2017YFA0504700), the Strategic Priority Research Program of CAS (XDB27020106, XDB08020302 and XDB08030204), the Key Research Program of Frontier Sciences of CAS (QYZDB-SSW-SMC005), and National Natural Science Foundation of China (grant numbers 31930064, 31770778, 31570724 and 31700649). Z.L. and X.Z received scholarships from the National Thousand (Young) Talents Program from the Office of Global Experts Recruitment in China.

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Author notes

  1. These authors contributed equally: Peng Cao, Duanfang Cao.

Authors and Affiliations

  1. National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, P. R. China

    Peng Cao, Duanfang Cao, Long Si, Xiaodong Su, Wenrui Chang, Zhenfeng Liu, Xinzheng Zhang & Mei Li

  2. University of Chinese Academy of Sciences, Beijing, P. R. China

    Long Si, Wenrui Chang, Zhenfeng Liu & Xinzheng Zhang

  3. Institute of Botany, Chinese Academy of Sciences, Beijing, P. R. China

    Lijin Tian

  4. Center for Biological Imaging, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, P. R. China

    Xinzheng Zhang

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  1. Peng Cao
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Contributions

M.L., W.C. and X.Z. conceived the project. P.C. performed the sample preparation and characterization. L.S. assisted with the sample preparation and characterization. D.C., P.C. and X.S. collected the cryo-EM data. D.C. and X.Z. processed the cryo-EM data and reconstructed the cryo-EM maps. P.C. built and refined the structure model. L.T. performed the PSI oxidation kinetics measurements. P.C., M.L., X.Z. and Z.L. analysed the structure and wrote the manuscript. All of the authors discussed and commented on the results and the manuscript.

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Correspondence to Xinzheng Zhang or Mei Li.

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Extended data

Extended Data Fig. 1 Sample preparation and characterization of the PSI3-IsiA18 and PSI3-IsiA18-Fld3 supercomplexes.

(a) Sucrose-density-gradient results of solubilized thylakoid membranes from cyanobacterial cells grown under normal conditions (PSI3, tube 1), iron-deficient conditions (PSI3-IsiA18, tube 2) and of cross-linked PSI3-IsiA18-Fld3 products (tube 3), respectively. The bands of PSI3, PSI3-IsiA18 and PSI3-IsiA18-Fld3 are labeled. Representative results were shown from three to ten independent samples. (b) Room-temperature absorption spectra of the PSI3-IsiA18, PSI3-IsiA18-Fld3 and PSI3 supercomplexes. Representative results were shown from ten independent samples. (c) Pigment content analysis of the PSI3-IsiA18 sample and the PSI3 sample by HPLC. The three major pigment peaks were identified as zeaxanthin (Zea), chlorophyll a (Chl a) and β-carotene (BCR). The HPLC measurements were repeated independently for three times with similar results obtained. (d) Gradient SDS-PAGE (4-20%) analysis of the PSI3-IsiA18-Fld3 and PSI3-IsiA18 samples. The protein composition of crosslinked Fld-PsaD band and other Coomassie bands are identified based on the mass spectrometry and proteomics data analysis. The representative result was shown from five replicates.

Source data

Extended Data Fig. 2

Cryo-EM data collection, refinement and validation statistics.

Extended Data Fig. 3 Structural comparison of the PSI3-IsiA18 and PSI3-IsiA18-Fld3 supercomplexes from Synechococcus 7942.

The PSI3-IsiA18 (cyan) and PSI3-IsiA18-Fld3 (orange) are superposed on one of the PsaA subunits. The Fld proteins are shown in cartoon mode. 1~6 indicates IsiA-1 to 6 in one monomer.

Extended Data Fig. 4 Structural comparison of the PSI3-IsiA18 supercomplexes from Synechococcus 7942 and Synechocystis 6803.

(a) The PSI3-IsiA18 supercomplex from Synechococcus 7942 (colored in magenta, yellow and pink for each of three monomers) and the PSI3-IsiA18 supercomplex from Synechocystis 6803 (PDB code 6NWA, colored in green) are superposed on one of the PsaA subunits. 1~6 indicates IsiA-1~6 in each monomer. (b) Enlarged view of one monomer containing PSI core and IsiA-1~6. The shift of IsiAs and the conformational change of PsaL between the two structures are indicated by red arrows.

Extended Data Fig. 5 The trimerization role of the C-terminal helix as well as the bound pigments and lipids in PsaL.

(a) Comparison of C-terminal helices of PsaL from Synechococcus 7942 (pink), Synechocystis 6803 (blue) and Anabaena 7120 (PDB code 6K61, cyan). (b, c) The distribution of pigments and lipids of PsaL from Synechococcus 7942 (b) and Synechocystis 6803 (PDB code 5OY0) (c) in the same luminal view and with the same scale. PsaL proteins are shown in cartoon and colored in pink, yellow and cyan for each monomer. The chlorophylls, carotenoids and lipids are shown as sticks. The BCR 4219 molecules of PsaL subunits in (b) are shown as spheres and indicated by black arrows.

Extended Data Fig. 6 The IsiA structure and the IsiA-IsiA’ interaction.

(a) Cartoon representation of IsiA. Helix I-VI and loops C and E are labeled. The chlorophylls a, carotenoids and the lipid molecule (sulfoquinovosyldiacyl glycerol, SQDG) are shown as sticks and colored green, orange and blue, respectively. The unique pigments bound with IsiA compared with PSII CP43 (a516, a517, a518, a519, BCR521) are shown in red color. (b) Structural superposition of IsiA from Synechococcus 7942 (warm pink) with IsiA from Synechocystis 6803 (white). (c) Structural superposition of IsiA (warm pink) with PSII CP43 (white, PDB code 3WU2). (d, e) The interactions between two adjacent IsiA proteins (warm pink, IsiA; light blue, IsiA’) from two different views. The pigments at the IsiA-IsiA’ interface are shown in sticks and labeled. The phytol chains of chlorophylls are omitted. The potential EET pathways are indicated by black dashes.

Extended Data Fig. 7 Interactions and potential EET pathways between IsiA-1~6 and PSI core.

(a-f) Side views of the interfaces between the core subunits and IsiA-1 (a), IsiA-2 (b), IsiA-3 (c), IsiA-4 (d), IsiA-5 (e) and IsiA-6 (f). Protein subunits and the interfacial pigments are shown in surface and stick modes, respectively. Potential EET pathways are shown by black dashed lines. The phytol chains of chlorophylls are omitted for clarity. PsaK1’ in (f) indicates the PsaK1 subunit from the neighboring PSI monomer.

Extended Data Fig. 8 Cytoplasmic view of IsiA dimers superposed on one IsiA monomer.

The “34” dimer is bent inwardly indicated by a black arrow.

Extended Data Fig. 9 Comparison of potential EET pathways between PSI3-IsiA18 supercomplexes from Synechococcus 7942 (a) and Synechocystis 6803 (b).

The two supercomplexes are viewed and colored as same as that in Fig. 6c. The potential pathways are indicated by dashed lines and the Mg-to-Mg distances are labelled by values (Å). The pathways with values colored in black represent the similar pathways with Mg-to-Mg distances < 20 Å in the two supercomplexes. The pathways with values colored in blue represent the pathways between IsiA-6 and PsaB, which differ greatly between the two supercomplexes (Mg-to-Mg distances > 20 Å in Synechococcus 7942, while Mg-to-Mg distances < 20 Å in Synechocystis 6803). The pathways with values colored in red represent the three pathways associated with Chl a1105PsaK in (a).

Extended Data Fig. 10 Functional antenna size of PSI3-IsiA18 and PSI3 supercomplexes from Synechococcus 7942.

(a, b) Effective PSI antenna sizes of PSI3-IsiA18 (blue) and PSI3 (red) were estimated by measuring the kinetics of P700 oxidation at two excitation wavelengths: 630 nm (a) and 720nm (b). The measurements were repeated independently for three times with similar results obtained. (c) The PSI oxidation kinetics was fitted with a mono-exponential model and the corresponding time constants were listed. The mean values and standard deviations were calculated from three independent measurements.

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Cao, P., Cao, D., Si, L. et al. Structural basis for energy and electron transfer of the photosystem I–IsiA–flavodoxin supercomplex. Nat. Plants 6, 167–176 (2020). https://doi.org/10.1038/s41477-020-0593-7

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