Skip to main content

Thank you for visiting 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.

Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria


Photosystem I (PSI) is present as trimeric complexes in most characterized cyanobacteria and as monomers in plants and algae. Recent reports of tetrameric PSI have raised questions regarding its structural basis, physiological role, phylogenetic distribution and evolutionary significance. Here, we examined PSI in 61 cyanobacteria, showing that tetrameric PSI, which correlates with the psaL gene and a distinct genomic structure, is widespread among heterocyst-forming cyanobacteria and their close relatives. Physiological studies revealed that expression of tetrameric PSI is favoured under high light, with an increased content of novel PSI-bound carotenoids (myxoxanthophyll, canthaxanthan and echinenone). In sum, this work suggests that tetrameric PSI is an adaptation to high light intensity, and that change in PsaL leads to monomerization of trimeric PSI, supporting the hypothesis of tetrameric PSI being the evolutionary intermediate in the transition from cyanobacterial trimeric PSI to monomeric PSI in plants and algae.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Examples of BN-PAGE and TEM analyses of PSI oligomeric states in different cyanobacteria.
Fig. 2: Distribution of PSI oligomers and the location of psaL genes among cyanobacteria with sequenced genomes.
Fig. 3: BN-PAGE and western blot analyses of PSI oligomers in Synechocystis sp. PCC 6803 expressing different PsaL.
Fig. 4: BN-PAGE analyses of cyanobacterial PSI oligomeric states under different light intensities.
Fig. 5: Comparison of TS-821 PSI oligomeric profiles under different light intensities.
Fig. 6: The impact of light intensities on tetrameric PSI in TS-821.

Data availability

The cloned cyanobacterial psaL sequences have been deposited in GenBank with the accession numbers KY575410, KY575411, KY575412, KY575413, KY575414, KY575415, KY575416, KY575417, KY575418, KY575419, KY575420, KY575421, KY575422, KY575423 and KY575424. The TS-821 whole-genome shotgun project has been deposited at DNA Data Bank of Japan/European Nucleotide Archive/GenBank under the accession MVDI00000000. The version described in this paper is version MVDI01000000.


  1. 1.

    Raymond, J. & Blankenship, R. E. in Advances in Photosynthesis and Respiration Vol. 24 (Ed. Goldbeck, J. H.) 669–681 (Springer, 2007).

  2. 2.

    Gardian, Z. et al. Organisation of photosystem i and photosystem iI in red alga Cyanidium caldarium: encounter of cyanobacterial and higher plant concepts. Biochim. Biophys. Acta 1767, 725–731 (2007).

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Watanabe, M., Kubota, H., Wada, H., Narikawa, R. & Ikeuchi, M. Novel supercomplex organization of photosystem I in Anabaena and Cyanophora paradoxa. Plant Cell Physiol. 52, 162–168 (2011).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Ben-Shem, A., Frolow, F. & Nelson, N. Crystal structure of plant photosystem I. Nature 426, 630–635 (2003).

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Kouril, R., van Oosterwijk, N., Yakushevska, A. E. & Boekema, E. J. Photosystem I: a search for green plant trimers. Photochem. Photobiol. Sci. 4, 1091–1094 (2005).

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Veith, T. & Buchel, C. The monomeric photosystem I-complex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes. Biochim. Biophys. Acta 1767, 1428–1435 (2007).

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Wood, W. H. J. et al. Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer. Nat. Plants 4, 116–12 (2018).

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Boekema, E. J. et al. Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett. 217, 283–286 (1987).

    CAS  Article  Google Scholar 

  9. 9.

    Shubin, V. V., Bezsmertnaya, I. N. & Karapetyan, N. V. Isolation from Spirulina membranes of 2 photosystem i-type complexes, one of which contains chlorophyll responsible for the 77-K fluorescence band at 760 Nm. FEBS Lett. 309, 340–342 (1992).

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Shubin, V. V., Tsuprun, V. L., Bezsmertnaya, I. N. & Karapetyan, N. V. Trimeric forms of the photosystem I reaction center complex pre‐exist in the membranes of the cyanobacterium Spirulina platensis. FEBS Lett. 334, 79–82 (1993).

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Tsiotis, G., Haase, W., Engel, A. & Michel, H. Isolation and structural characterization of trimeric cyanobacterial photosystem I complex with the help of recombinant antibody fragments. Eur. J. Biochem. 231, 823–830 (1995).

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    Garczarek, L., van der Staay, G. W. M., Thomas, J. C. & Partensky, F. Isolation and characterization of photosystem I from two strains of the marine oxychlorobacterium Prochlorococcus. Photosynth. Res. 56, 131–141 (1998).

    CAS  Article  Google Scholar 

  13. 13.

    Bibby, T. S., Mary, I., Nield, J., Partensky, F. & Barber, J. Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature 424, 1051–1054 (2003).

    CAS  PubMed  Article  Google Scholar 

  14. 14.

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

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Tucker, D. L. & Sherman, L. A. Analysis of chlorophyll–protein complexes from the cyanobacterium Cyanothece sp. ATCC 51142 by non-denaturing gel electrophoresis. Biochim. et Biophys. 1468, 150–160 (2000).

    CAS  Article  Google Scholar 

  16. 16.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Mangels, D. et al. Photosystem I from the unusual cyanobacterium Gloeobacter violaceus. Photosynth. Res. 72, 307–319 (2002).

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Almog, O., Shoham, G., Michaeli, D. & Nechushtai, R. Monomeric and trimeric forms of photosystem I reaction center of Mastigocladus laminosus: crystallization and preliminary characterization. Proc. Natl Acad. Sci. USA 88, 5312–5316 (1991).

    CAS  PubMed  Article  Google Scholar 

  20. 20.

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

    CAS  PubMed  Article  Google Scholar 

  21. 21.

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

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Semchonok, D. A., Li, M., Bruce, B. D., Oostergetel, G. T. & Boekema, E. J. Cryo-EM structure of a tetrameric cyanobacterial photosystem I complex reveals novel subunit interactions. Biochim. Biophys. Acta 1857, 1619–1626 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. 24.

    Malavath, T., Caspy, I., Netzer-El, S. Y., Klaiman, D. & Nelson, N. Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis. Biochim. Biophys. Acta 1859, 645–654 (2018).

    CAS  Article  Google Scholar 

  25. 25.

    Gan, F. et al. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345, 1312–1317 (2014).

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Gan, F. & Bryant, D. A. Adaptive and acclimative responses of cyanobacteria to far-red light. Environ. Microbiol. 17, 3450–3465 (2015).

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    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  PubMed  Article  Google Scholar 

  28. 28.

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  29. 29.

    Cardona, T. et al. Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochim. Biophys. Acta 1787, 252–263 (2009).

    CAS  PubMed  Article  Google Scholar 

  30. 30.

    Vintila, S. & El-Shehawy, R. Ammonium ions inhibit nitrogen fixation but do not affect heterocyst frequency in the bloom-forming cyanobacterium Nodularia spumigena strain AV1. Microbiology 153, 3704–3712 (2007).

    CAS  PubMed  Article  Google Scholar 

  31. 31.

    Vintila, S. & El-Shehawy, R. Variability in the response of the cyanobacterium Nodularia spumigena to nitrogen supplementation. J. Environ. Monit. 12, 1885–1890 (2010).

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1–61 (1979).

    Google Scholar 

  33. 33.

    Fewer, D., Friedl, T. & Budel, B. Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other’s closest living relatives. Mol. Phylogenet. Evol. 23, 82–90 (2002).

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Shih, P. M. et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl Acad. Sci. USA 110, 1053–1058 (2013).

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Iwuchukwu, I. J. et al. Self-organized photosynthetic nanoparticle for cell-free hydrogen production. Nat. Nanotechnol. 5, 73–79 (2010).

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Baker, D. R. et al. Comparative photoactivity and stability of isolated cyanobacterial monomeric and trimeric photosystem I. J. Phys. Chem. B 118, 2703–2711 (2014).

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Wang, Q. et al. The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol. 147, 1239–1250 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. 38.

    Dagan, T. et al. Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol. Evol. 5, 31–44 (2013).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  39. 39.

    Sánchez-Baracaldo, P., Raven, J. A., Pisani, D. & Knoll, A. H. Early photosynthetic eukaryotes inhabited low-salinity habitats. Proc. Natl Acad. Sci. USA 114, E7737–E7745 (2017).

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Ponce-Toledo, R. I. et al. An early-branching freshwater cyanobacterium at the origin of plastids. Curr. Biol. 27, 386–391 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Amunts, A. & Nelson, N. Plant photosystem I design in the light of evolution. Structure 17, 637–650 (2009).

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Alboresi, A. et al. Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana. New Phytol. 213, 714–726 (2017).

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Watanabe, M., Iwai, M., Narikawa, R. & Ikeuchi, M. Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol. 50, 1674–1680 (2009).

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Iwamura, T., Nagai, H. & Ichimura, S.-E. Improved methods for determining contents of chlorophyll, protein, bibonucleic acid, and deoxyribonucleic acid in planktonic populations. Int. Rev. ges. Hydrobiol. Hydrogr. 55, 131–147 (1970).

    CAS  Article  Google Scholar 

  45. 45.

    Schägger, H. & von Jagow, G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223–231 (1991).

    PubMed  Article  Google Scholar 

  46. 46.

    Wittig, I., Braun, H.-P. & Schagger, H. Blue native PAGE. Nat. Protoc. 1, 418–428 (2006).

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Kolaskar, A. S. & Tongaonkar, P. C. A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Lett. 276, 172–174 (1990).

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Saha, S. & Raghava, G. P. S. Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins 65, 40–48 (2006).

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Wattam, A. R. et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 42, D581–D591 (2014).

    CAS  PubMed  Article  Google Scholar 

  51. 51.

    Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206–D214 (2014).

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Calteau, A. et al. Phylum-wide comparative genomics unravel the diversity of secondary metabolism in cyanobacteria. BMC Genomics 15, 977 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  53. 53.

    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  55. 55.

    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. ProtTest 3: Fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164–1165 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: An online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. 58.

    Vallenet, D. et al. MicroScope in 2017: An expanding and evolving integrated resource for community expertise of microbial genomes. Nucleic Acids Res. 45, D517–D528 (2017).

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Schirrmeister, B. E., Gugger, M. & Donoghue, P. C. Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils. Palaeontology 58, 769–785 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: A sequence logo generator. Genome Res. 14, 1188–1190 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references


Support to B.D.B., M.L. and J.T.N. was provided by the Gibson Family Foundation, the Bredesen Center for Interdisciplinary Research and Education, the Tennessee Plant Research Center, a UTK Professional Development Award, the Dr. Donald L. Akers Faculty Enrichment Fellowship to B.D.B. and National Science Foundation support to B.D.B. (DGE-0801470 and EPS-1004083). M.L. has been supported as a CIRE Fellow at University of Tennessee, Knoxville. A Professional Development Award from the Graduate School at UTK supported travel of B.D.B. to the Netherlands and to the Institut Pasteur. NWO Chemical Sciences supported work at University of Groningen. J.P.W. has been supported by NIH P30 DK063491. The Institut Pasteur supported Pasteur Culture Collection of cyanobacteria. We thank Y. I. Park for the use of the cyanobacterial genome of PCC 7124, and N.G. Brady and T. Cardona for helpful comments on the manuscript.

Author information




M.L., M.G. and B.D.B. designed the research. M.L. carried out most of the biochemistry and molecular biology experiments. A.C. performed phylogenetic and bioinformatics analyses. D.A.S. and E.J.B. did the electron microscopy imaging and single-particle analyses. T.A.W. did most of the psaL cloning. N.S. and J.T.N. prepared most of the cell materials. J.T.N. carried out the spectral comparison of PCC 7414 PSI oligomers J.W. performed the proteomic analyses. M.L. and B.D.B. wrote the article and all other authors contributed in editing and revising the article.

Corresponding author

Correspondence to Barry D. Bruce.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Conrad Mullineaux, Ann Magnuson and the other, anonymous, reviewer 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. 1–10 and Supplementary Tables 1 and 2.

Reporting Summary

Supplementary Data 1

PSI oligomeric states in cyanobacteria studied, Cyanobacteria culture conditions and genome sequences used in this study.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, M., Calteau, A., Semchonok, D.A. et al. Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria. Nat. Plants 5, 1309–1319 (2019).

Download citation

Further reading


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