Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I

Abstract

In plants and green algae, the core of photosystem I (PSI) is surrounded by a peripheral antenna system consisting of light-harvesting complex I (LHCI). Here we report the cryo-electron microscopic structure of the PSI–LHCI supercomplex from the green alga Chlamydomonas reinhardtii. The structure reveals that eight Lhca proteins form two tetrameric LHCI belts attached to the PsaF side while the other two Lhca proteins form an additional Lhca2/Lhca9 heterodimer attached to the opposite side. The spatial arrangement of light-harvesting pigments reveals that Chlorophylls b are more abundant in the outer LHCI belt than in the inner LHCI belt and are absent from the core, thereby providing the downhill energy transfer pathways to the PSI core. PSI–LHCI is complexed with a plastocyanin on the patch of lysine residues of PsaF at the luminal side. The assembly provides a structural basis for understanding the mechanism of light-harvesting, excitation energy transfer of the PSI–LHCI supercomplex and electron transfer with plastocyanin.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Cryo-EM structure of the PSI–LHCI supercomplex from C. reinhardtii.
Fig. 2: Cryo-EM density map and structure of the Lhca2/Lhca9 heterodimer.
Fig. 3: Comparison of the structures of five LHCI heterodimers.
Fig. 4: Comparison of the structures of green algal PSI–LHCI and red algal PSI–LHCR.
Fig. 5: Distribution of Chls a and b in green algal PSI–LHCI.
Fig. 6: Chlorophyll arrangement and plausible energy transfer pathways in the PSI–LHCI supercomplex.
Fig. 7: Extra density in the vicinity of the N-terminal helix of PsaF at the luminal side.

Data availability

Atomic coordinates of the green algal PSI–LHCI have been deposited in the Protein Data Bank with accession codes 6JO5 (PSI–10Lhca) and 6JO6 (PSI–8Lhca). Cryo-EM maps of green algal PSI–LHCI have been deposited in the Electron Microscopy Data Bank with accession codes EMD-9853 (map c2), EMD-9854 (map d), EMD-9855 (map a) and EMD-9856 (map b).

References

  1. 1.

    Nelson, N. & Junge, W. Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu. Rev. Biochem. 84, 659–683 (2015).

  2. 2.

    Suga, M., Qin, X., Kuang, T. & Shen, J. R. Structure and energy transfer pathways of the plant photosystem I-LHCI supercomplex. Curr. Opin. Struct. Biol. 39, 46–53 (2016).

    CAS  Article  Google Scholar 

  3. 3.

    Nelson, N. Plant photosystem I - the most efficient nano-photochemical machine. J. Nanosci. Nanotechnol. 9, 1709–1713 (2009).

    CAS  Article  Google Scholar 

  4. 4.

    Hippler, M., Drepper, F., Haehnel, W. & Rochaix, J. D. The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 95, 7339–7344 (1998).

    CAS  Article  Google Scholar 

  5. 5.

    Hippler, M., Drepper, F., Rochaix, J. D. & Muhlenhoff, U. Insertion of the N-terminal part of PsaF from Chlamydomonas reinhardtii into photosystem I from Synechococcus elongatus enables efficient binding of algal plastocyanin and cytochrome c6. J. Biol. Chem. 274, 4180–4188 (1999).

    CAS  Article  Google Scholar 

  6. 6.

    Kubota-Kawai, H. et al. X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex. Nat. Plants 4, 218–224 (2018).

    CAS  Article  Google Scholar 

  7. 7.

    Blankenship, R. E. Origin and early evolution of photosynthesis. Photosynth. Res. 33, 91–111 (1992).

    CAS  Article  Google Scholar 

  8. 8.

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

    CAS  Article  Google Scholar 

  9. 9.

    Mazor, Y., Borovikova, A., Caspy, I. & Nelson, N. Structure of the plant photosystem I supercomplex at 2.6 A resolution. Nat. Plants 3, 17014 (2017).

    CAS  Article  Google Scholar 

  10. 10.

    Qin, X., Suga, M., Kuang, T. & Shen, J. R. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348, 989–995 (2015).

    CAS  Article  Google Scholar 

  11. 11.

    Mazor, Y., Borovikova, A. & Nelson, N. The structure of plant photosystem I super-complex at 2.8 A resolution. eLife 4, e07433 (2015).

    Article  Google Scholar 

  12. 12.

    Pan, X. W., Liu, Z. F., Li, M. & Chang, W. R. Architecture and function of plant light-harvesting complexes II. Curr. Opin. Struct. Biol. 23, 515–525 (2013).

    CAS  Article  Google Scholar 

  13. 13.

    Drop, B. et al. Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J. Biol. Chem. 286, 44878–44887 (2011).

    CAS  Article  Google Scholar 

  14. 14.

    Ozawa, S. et al. Configuration of ten light-harvesting chlorophyll a/b complex I subunits in Chlamydomonas reinhardtii photosystem I. Plant Physiol. 178, 583–595 (2018).

  15. 15.

    Kubota-Kawai, H. et al. Ten antenna proteins are associated with the core in the supramolecular organization of the photosystem I supercomplex in Chlamydomonas reinhardtii. J. Biol. Chem. 294, 4304–4314 (2019).

    CAS  Article  Google Scholar 

  16. 16.

    Su, X. et al. Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex. Nat. Plants 5, 273–281 (2019).

    Article  Google Scholar 

  17. 17.

    Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).

    CAS  Article  Google Scholar 

  18. 18.

    Watanabe, A., Kim, E., Burton-Smith, R. N., Tokutsu, R. & Minagawa, J. Amphipol-assisted purification method for the highly active and stable photosystem II supercomplex of Chlamydomonas reinhardtii. FEBS Lett. 593, 1072–1079 (2019).

    CAS  Article  Google Scholar 

  19. 19.

    Ozawa, S., Kosugi, M., Kashino, Y., Sugimura, T. & Takahashi, Y. 5′-Monohydroxyphylloquinone is the dominant naphthoquinone of PSI in the green alga Chlamydomonas reinhardtii . Plant Cell Physiol. 53, 237–243 (2012).

    CAS  Article  Google Scholar 

  20. 20.

    Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428, 287–292 (2004).

    CAS  Article  Google Scholar 

  21. 21.

    Pan, X. et al. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat. Struct. Mol. Biol. 18, 309–315 (2011).

    CAS  Article  Google Scholar 

  22. 22.

    Wei, X. et al. Structure of spinach photosystem II-LHCII supercomplex at 3.2 A resolution. Nature 534, 69–74 (2016).

    CAS  Article  Google Scholar 

  23. 23.

    Bujaldon, S. et al. Functional accumulation of antenna proteins in chlorophyll b-less mutants of Chlamydomonas reinhardtii. Mol. Plant 10, 115–130 (2017).

    CAS  Article  Google Scholar 

  24. 24.

    Qin, X. et al. Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat. Plants 5, 263–272 (2019).

    Article  Google Scholar 

  25. 25.

    Fan, M. et al. Crystal structures of the PsbS protein essential for photoprotection in plants. Nat. Struct. Mol. Biol. 22, 729–735 (2015).

    CAS  Article  Google Scholar 

  26. 26.

    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).

    CAS  Article  Google Scholar 

  27. 27.

    Pi, X. et al. Unique organization of photosystem I-light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc. Natl Acad. Sci. USA 115, 4423–4428 (2018).

    CAS  Article  Google Scholar 

  28. 28.

    Pan, X. et al. Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II. Science 360, 1109–1113 (2018).

    CAS  Article  Google Scholar 

  29. 29.

    Shimada, S. et al. Complex structure of cytochrome c-cytochrome c oxidase reveals a novel protein-protein interaction mode. EMBO J. 36, 291–300 (2016).

    Article  Google Scholar 

  30. 30.

    Fischer, N., Stampacchia, O., Redding, K. & Rochaix, J. D. Selectable marker recycling in the chloroplast. Mol. Gen. Genet. 251, 373–380 (1996).

    CAS  Article  Google Scholar 

  31. 31.

    Kuroda, H., Kodama, N., Sun, X. Y., Ozawa, S. & Takahashi, Y. Requirement for Asn298 on D1 protein for oxygen evolution: analyses by exhaustive amino acid substitution in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol. 55, 1266–1275 (2014).

    CAS  Article  Google Scholar 

  32. 32.

    Ozawa, S. et al. Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21, 2424–2442 (2009).

    CAS  Article  Google Scholar 

  33. 33.

    Chua, N. H. & Bennoun, P. Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl Acad. Sci. USA 72, 2175–2179 (1975).

    CAS  Article  Google Scholar 

  34. 34.

    Fling, S. P. & Gregerson, D. S. Peptide and protein molecular weight determination by electrophoresis using a high-molarity Tris buffer system without urea. Anal. Biochem. 155, 83–88 (1986).

    CAS  Article  Google Scholar 

  35. 35.

    Ozawa, S., Onishi, T. & Takahashi, Y. Identification and characterization of an assembly intermediate subcomplex of photosystem I in the green alga Chlamydomonas reinhardtii. J. Biol. Chem. 285, 20072–20079 (2010).

    CAS  Article  Google Scholar 

  36. 36.

    Yamano, T. et al. Light and low-CO2-dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol. 51, 1453–1468 (2010).

    CAS  Article  Google Scholar 

  37. 37.

    Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).

    CAS  Article  Google Scholar 

  38. 38.

    Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).

    CAS  Article  Google Scholar 

  39. 39.

    Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).

    CAS  Article  Google Scholar 

  40. 40.

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

    CAS  Article  Google Scholar 

  41. 41.

    Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).

    Article  Google Scholar 

  42. 42.

    Adams, P. D. et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank J.-R. Shen and K. Iwasaki for discussions, especially at the initial stage of the project. We also thank A. Watanabe, R. Tokutsu and J. Minagawa at the National Institute for Basic Biology for the valuable suggestion to use Amphipol in the PSI-LHCI preparations. This research was supported by the Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research) from AMED. This work was supported by JSPS KAKENHI (grant nos. JP16H06162 and JP16H06296 to M.S. and JP16H06554 to Y.T.). This work was also supported by JST, PREST (grant no. JP18069982 to M.S.).

Author information

Affiliations

Authors

Contributions

M.S., N.M. and Y.T. conceived the project. S.-I.O. and K.Y.-M. prepared the samples. N.M. and F.A. collected the cryo-EM data. N.M. processed the cryo-EM data. M.S. built and refined the structure. M.S., S.-I.O. and Y.T. wrote the manuscript. All authors discussed and commented on the results and the manuscript.

Corresponding authors

Correspondence to Naoyuki Miyazaki or Yuichiro Takahashi.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer Review Information: Nature Plants thanks Alexey Amunts, Jean-David Rochaix and other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–13, Supplementary Tables 1–7.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Suga, M., Ozawa, SI., Yoshida-Motomura, K. et al. Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I. Nat. Plants 5, 626–636 (2019). https://doi.org/10.1038/s41477-019-0438-4

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing