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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.

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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.

References

  1. Liu, L. N. Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta 1857, 256–265 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Vermaas, W. F. in Encyclopedia of Life Sciences 245–251 (Nature Publishing Group, 2001).

  3. Mullineaux, C. W. Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta 1837, 503–511 (2014).

    Article  CAS  PubMed  Google Scholar 

  4. Saer, R. G. & Blankenship, R. E. Light harvesting in phototrophic bacteria: structure and function. Biochem. J. 474, 2107–2131 (2017).

    Article  CAS  PubMed  Google Scholar 

  5. Chen, H.-Y. S., Bandyopadhyay, A. & Pakrasi, H. B. Function, regulation and distribution of IsiA, a membrane-bound chlorophyll a-antenna protein in cyanobacteria. Photosynthetica 56, 322–333 (2018).

    Article  CAS  Google Scholar 

  6. Bibby, T. S., Nield, J. & Barber, J. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412, 743–745 (2001).

    Article  CAS  PubMed  Google Scholar 

  7. Boekema, E. J. et al. A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412, 745–748 (2001).

    Article  CAS  PubMed  Google Scholar 

  8. Vinnemeier, J., Kunert, A. & Hagemann, M. Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Lett. 169, 323–330 (1998).

    Article  CAS  PubMed  Google Scholar 

  9. Havaux, M. et al. The chlorophyll-binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Lett. 579, 2289–2293 (2005).

    Article  CAS  PubMed  Google Scholar 

  10. Yousef, N., Pistorius, E. K. & Michel, K. P. Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild-type and selected mutants. Arch. Microbiol. 180, 471–483 (2003).

    Article  CAS  PubMed  Google Scholar 

  11. Toporik, H., Li, J., Williams, D., Chiu, P. L. & Mazor, Y. The structure of the stress-induced photosystem I-IsiA antenna supercomplex. Nat. Struct. Mol. Biol. 26, 443–449 (2019).

    Article  CAS  PubMed  Google Scholar 

  12. Cao, P. et al. Structural basis for energy and electron transfer of the photosystem I-IsiA-flavodoxin supercomplex. Nat. Plants 6, 167–176 (2020).

    Article  CAS  PubMed  Google Scholar 

  13. Ma, F. et al. Dynamic changes of IsiA-containing complexes during long-term iron deficiency in Synechocystis sp PCC 6803. Mol. Plant 10, 143–154 (2017).

    Article  CAS  PubMed  Google Scholar 

  14. Sun, J. L. & Golbeck, J. H. The presence of the IsiA–PSI supercomplex leads to enhanced photosystem I electron throughput in iron-starved cells of Synechococcus sp. PCC 7002. J. Phys. Chem. B 119, 13549–13559 (2015).

    Article  CAS  PubMed  Google Scholar 

  15. Chauhan, D. et al. A novel photosynthetic strategy for adaptation to low-iron aquatic environments. Biochemistry 50, 686–692 (2011).

    Article  CAS  PubMed  Google Scholar 

  16. Park, Y. I., Sandstrom, S., Gustafsson, P. & Oquist, G. Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation. Mol. Microbiol 32, 123–129 (1999).

    Article  CAS  PubMed  Google Scholar 

  17. Schoffman, H. & Keren, N. Function of the IsiA pigment-protein complex in vivo. Photosynth. Res. 141, 343–353 (2019).

  18. Busch, K. B., Deckers-Hebestreit, G., Hanke, G. T. & Mulkidjanian, A. Y. Dynamics of bioenergetic microcompartments. Biol. Chem. 394, 163–188 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Casella, S. et al. Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery. Mol. Plant 10, 1434–1448 (2017).

    Article  CAS  PubMed  Google Scholar 

  20. MacGregor-Chatwin, C. et al. Lateral segregation of photosystem I in cyanobacterial thylakoids. Plant Cell 29, 1119–1136 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bečková, M. et al. Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to high light. Mol. Plant 10, 62–72 (2017).

    Article  PubMed  CAS  Google Scholar 

  22. Liu, H. et al. Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342, 1104–1107 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Liu, L. N. & Scheuring, S. Investigation of photosynthetic membrane structure using atomic force microscopy. Trends Plant Sci. 18, 277–286 (2013).

    Article  CAS  PubMed  Google Scholar 

  24. MacGregor-Chatwin, C. et al. Membrane organization of photosystem I complexes in the most abundant phototroph on Earth. Nat. Plants 5, 879–889 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Riediger, M. et al. Biocomputational analyses and experimental validation identify the regulon controlled by the redox-responsive transcription factor RpaB. iScience 15, 316–331 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kappell, A. D., Bhaya, D. & van Waasbergen, L. G. Negative control of the high light-inducible hliA gene and implications for the activities of the NblS sensor kinase in the cyanobacterium Synechococcus elongatus strain PCC 7942. Arch. Microbiol. 186, 403–413 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Liu, L. N. et al. Control of electron transport routes through redox-regulated redistribution of respiratory complexes. Proc. Natl Acad. Sci. USA 109, 11431–11436 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sun, Y. et al. Light modulates the biosynthesis and organization of cyanobacterial carbon fixation machinery through photosynthetic electron flow. Plant Physiol. 171, 530–541 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sun, Y., Wollman, A. J. M., Huang, F., Leake, M. C. & Liu, L. N. Single-organelle quantification reveals the stoichiometric and structural variability of carboxysomes dependent on the environment. Plant Cell 31, 1648–1664 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411, 909–917 (2001).

    Article  CAS  PubMed  Google Scholar 

  31. Yeremenko, N. et al. Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43, 10308–10313 (2004).

    Article  CAS  PubMed  Google Scholar 

  32. Zipfel, W. & Owens, T. G. Calculation of absolute photosystem I absorption cross-sections from P700 photo-oxidation kinetics. Photosynth. Res. 29, 23–35 (1991).

    CAS  PubMed  Google Scholar 

  33. Ryan-Keogh, T. J., Macey, A. I., Cockshutt, A. M., Moore, C. M. & Bibby, T. S. The cyanobacterial chlorophyll-binding-protein Isia acts to increase the in vivo effective absorption cross-section of PSI under iron limitation. J. Phycol. 48, 145–154 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Odom, W. R., Hodges, R., Chitnis, P. R. & Guikema, J. A. Characterization of Synechocystis sp. PCC 6803 in iron-supplied and iron-deficient media. Plant Mol. Biol. 23, 1255–1264 (1993).

    Article  CAS  PubMed  Google Scholar 

  35. Yadav, K. N. et al. Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH. Biochim. Biophys. Acta Bioenerg. 1858, 12–20 (2017).

    Article  CAS  PubMed  Google Scholar 

  36. Steinbeck, J. et al. Structure of a PSI-LHCI-cyt b6f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions. Proc. Natl Acad. Sci. USA 115, 10517–10522 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Rast, A. et al. Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane. Nat. Plants 5, 436–446 (2019).

    Article  CAS  PubMed  Google Scholar 

  38. Hellmich, J. et al. Native-like photosystem II superstructure at 2.44 A resolution through detergent extraction from the protein crystal. Structure 22, 1607–1615 (2014).

    Article  CAS  PubMed  Google Scholar 

  39. Umena, Y., Kawakami, K., Shen, J. R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473, 55–60 (2011).

    Article  CAS  PubMed  Google Scholar 

  40. Chang, L. et al. Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res. 25, 726–737 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zlenko, D. V., Galochkina, T. V., Krasilnikov, P. M. & Stadnichuk, I. N. Coupled rows of PBS cores and PSII dimers in cyanobacteria: symmetry and structure. Photosynth. Res. 133, 245–260 (2017).

    Article  CAS  PubMed  Google Scholar 

  42. McConnell, M. D., Koop, R., Vasil’ev, S. & Bruce, D. Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol. 130, 1201–1212 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Seelert, H., Dencher, N. A. & Müller, D. J. Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J. Mol. Biol. 333, 337–344 (2003).

    Article  CAS  PubMed  Google Scholar 

  44. Hahn, A., Vonck, J., Mills, D. J., Meier, T. & Kuhlbrandt, W. Structure, mechanism, and regulation of the chloroplast ATP synthase. Science 360, eaat4318 (2018).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  45. Pogoryelov, D. et al. The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. J. Bacteriol. 189, 5895–5902 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Strauss, M., Hofhaus, G., Schroder, R. R. & Kuhlbrandt, W. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27, 1154–1160 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Daum, B., Nicastro, D., Il, J. A., McIntosh, J. R. & Kuhlbrandt, W. Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22, 1299–1312 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Schuller, J. M. et al. Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer. Science 363, 257–260 (2019).

    Article  PubMed  CAS  Google Scholar 

  49. Laughlin, T. G., Bayne, A. N., Trempe, J. F., Savage, D. F. & Davies, K. M. Structure of the complex I-like molecule NDH of oxygenic photosynthesis. Nature 566, 411–414 (2019).

    Article  PubMed  CAS  Google Scholar 

  50. Arteni, A. A. et al. Structural characterization of NDH-1 complexes of Thermosynechococcus elongatus by single particle electron microscopy. Biochim. Biophys. Acta 1757, 1469–1475 (2006).

    Article  CAS  PubMed  Google Scholar 

  51. Folea, I. M. et al. Single particle analysis of thylakoid proteins from Thermosynechococcus elongatus and Synechocystis 6803: localization of the CupA subunit of NDH-1. FEBS Lett. 582, 249–254 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Birungi, M. et al. Possibilities of subunit localization with fluorescent protein tags and electron microscopy examplified by a cyanobacterial NDH-1 study. Biochim. Biophys. Acta 1797, 1681–1686 (2010).

    Article  CAS  PubMed  Google Scholar 

  53. Peltier, G., Aro, E. M. & Shikanai, T. NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu. Rev. Plant Biol. 67, 55–80 (2016).

    Article  CAS  PubMed  Google Scholar 

  54. Schuller, J. M. et al. Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I. Nat. Commun. 11, 494 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Pan, X. et al. Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nat. Commun. 11, 610 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhang, C. et al. Structural insights into NDH-1 mediated cyclic electron transfer. Nat. Commun. 11, 888–888 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kouril, R. et al. Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J. 77, 568–576 (2014).

    Article  CAS  PubMed  Google Scholar 

  58. Peng, L., Fukao, Y., Fujiwara, M., Takami, T. & Shikanai, T. Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21, 3623–3640 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Gao, F. et al. The NDH–1L-PSI supercomplex is important for efficient cyclic electron transport in cyanobacteria. Plant Physiol. 172, 1451–1464 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Singh, A. K. & Sherman, L. A. Iron-independent dynamics of IsiA production during the transition to stationary phase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Lett. 256, 159–164 (2006).

    Article  CAS  PubMed  Google Scholar 

  61. Bibby, T. S., Nield, J. & Barber, J. Three-dimensional model and characterization of the iron stress-induced CP43’-photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 276, 43246–43252 (2001).

    Article  CAS  PubMed  Google Scholar 

  62. Kouril, R. et al. Photosystem I trimers from Synechocystis PCC 6803 lacking the PsaF and PsaJ subunits bind an IsiA ring of 17 units. Biochim. Biophys. Acta 1607, 1–4 (2003).

    Article  CAS  PubMed  Google Scholar 

  63. Aspinwall, C. L., Duncan, J., Bibby, T., Mullineaux, C. W. & Barber, J. The trimeric organisation of photosystem I is not necessary for the iron-stress induced CP43' protein to functionally associate with this reaction centre. FEBS Lett. 574, 126–130 (2004).

    Article  CAS  PubMed  Google Scholar 

  64. Kouril, R. et al. Supercomplexes of IsiA and photosystem I in a mutant lacking subunit PsaL. Biochim. Biophys. Acta 1706, 262–266 (2005).

    Article  CAS  PubMed  Google Scholar 

  65. Sarcina, M. & Mullineaux, C. W. Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J. Biol. Chem. 279, 36514–36518 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Riethman, H. C. & Sherman, L. A. Purification and characterization of an iron stress-induced chlorophyll-protein from the cyanobacterium Anacystis nidulans R2. Biochim. Biophys. Acta 935, 141–151 (1988).

    Article  CAS  PubMed  Google Scholar 

  67. Burnap, R. L., Troyan, T. & Sherman, L. A. The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43') is encoded by the isiA gene. Plant Physiol. 103, 893–902 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Sandstrom, S., Park, Y. I., Oquist, G. & Gustafsson, P. CP43’, the isiA gene product, functions as an excitation energy dissipator in the cyanobacterium Synechococcus sp. PCC 7942. Photochem. Photobiol. 74, 431–437 (2001).

    Article  CAS  PubMed  Google Scholar 

  69. Zhang, J. et al. Structure of phycobilisome from the red alga Griffithsia pacifica. Nature 551, 57–63 (2017).

    Article  CAS  PubMed  Google Scholar 

  70. Liu, L. N., Chen, X. L., Zhang, Y. Z. & Zhou, B. C. Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacteria and red algae: An overview. Biochim. Biophys. Acta Bioenerg. 1708, 133–142 (2005).

    Article  CAS  Google Scholar 

  71. Arteni, A. A. et al. Structure and organization of phycobilisomes on membranes of the red alga Porphyridium cruentum. Photosynth. Res. 95, 169–174 (2008).

    Article  CAS  PubMed  Google Scholar 

  72. Liu, L. N. et al. Light-induced energetic decoupling as a mechanism for phycobilisome-related energy dissipation in red algae: a single molecule study. PLoS ONE 3, e3134 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Zhao, L. S. et al. Supramolecular architecture of photosynthetic membrane in red algae in response to nitrogen starvation. Biochim. Biophys. Acta 1857, 1751–1758 (2016).

    Article  CAS  PubMed  Google Scholar 

  74. Green, B. R. What happened to the phycobilisome? Biomolecules 9, 748 (2019).

  75. Straskova, A. et al. Pigment-protein complexes are organized into stable microdomains in cyanobacterial thylakoids. Biochim. Biophys. Acta Bioenerg. 1860, 148053 (2019).

  76. Folea, I. M., Zhang, P., Aro, E. M. & Boekema, E. J. Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett. 582, 1749–1754 (2008).

    Article  CAS  PubMed  Google Scholar 

  77. Liu, L. N. et al. Watching the native supramolecular architecture of photosynthetic membrane in red algae: topography of phycobilisomes and their crowding, diverse distribution patterns. J. Biol. Chem. 283, 34946–34953 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Lenn, T., Leake, M. C. & Mullineaux, C. W. Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo. Mol. Microbiol. 70, 1397–1407 (2008).

    Article  CAS  PubMed  Google Scholar 

  79. Llorente-Garcia, I. et al. Single-molecule in vivo imaging of bacterial respiratory complexes indicates delocalized oxidative phosphorylation. Biochim. Biophys. Acta 1837, 811–824 (2014).

    Article  CAS  PubMed  Google Scholar 

  80. Johnson, A. S., van Horck, S. & Lewis, P. J. Dynamic localization of membrane proteins in Bacillus subtilis. Microbiology 150, 2815–2824 (2004).

    Article  CAS  PubMed  Google Scholar 

  81. Cornejo, E., Abreu, N. & Komeili, A. Compartmentalization and organelle formation in bacteria. Curr. Opin. Cell Biol. 26, 132–138 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Vogel, F., Bornhovd, C., Neupert, W. & Reichert, A. S. Dynamic subcompartmentalization of the mitochondrial inner membrane. J. Cell Biol. 175, 237–247 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Watanabe, M. et al. Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc. Natl Acad. Sci. USA 111, 2512–2517 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Iwai, M. et al. Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464, 1210–1213 (2010).

    Article  CAS  PubMed  Google Scholar 

  85. Peng, L., Shimizu, H. & Shikanai, T. The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283, 34873–34879 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Lapuente-Brun, E. et al. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340, 1567–1570 (2013).

    Article  CAS  PubMed  Google Scholar 

  87. Katoh, H., Grossman, A. R., Hagino, N. & Ogawa, T. A gene of Synechocystis sp strain PCC 6803 encoding a novel iron transporter. J. Bacteriol. 182, 6523–6524 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wang, Q., Hall, C. L., Al-Adami, M. Z. & He, Q. IsiA is required for the formation of photosystem I supercomplexes and for efficient state transition in synechocystis PCC 6803. PLoS ONE 5, e10432 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Gust, B., Kieser, T. & Chater, K. F. REDIRECT Technology: PCR-targeting System in Streptomyces coelicolor (John Innes Centre, 2002).

  90. Huang, F. et al. Roles of RbcX in carboxysome biosynthesis in the cyanobacterium Synechococcus elongatus PCC7942. Plant Physiol. 179, 184–194 (2019).

    Article  CAS  PubMed  Google Scholar 

  91. Li, M., Semchonok, D. A., Boekema, E. J. & Bruce, B. D. Characterization and evolution of tetrameric photosystem I from the thermophilic cyanobacterium Chroococcidiopsis sp TS-821. Plant Cell 26, 1230–1245 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Zhang, P. P. et al. Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803. Plant Cell 16, 3326–3340 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article  CAS  PubMed  Google Scholar 

  94. Zhang, P. P. et al. Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24, 1952–1971 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Faulkner, M. et al. Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes. Nanoscale 9, 10662–10673 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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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 2

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Supplementary Data File 3

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

Supplementary Data File 4

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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.

Supplementary Data File 8

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Supplementary Data File 9

Statistical source data for Supplementary Table 1.

Supplementary Data File 10

Statistical source data for Supplementary Table 2.

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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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