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Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria

Nature Plants volume 5, pages 1309–1319 (2019)Cite this article

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Abstract

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.

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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.

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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.

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Acknowledgements

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.

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Author notes

  1. Meng Li

    Present address: School of Oceanography, University of Washington, Seattle, WA, USA

Authors and Affiliations

  1. Biochemistry and Cellular and Molecular Biology Department, University of Tennessee, Knoxville, TN, USA

    Meng Li, Thomas A. Witt, Jonathan T. Nguyen & Barry D. Bruce

  2. Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville, TN, USA

    Meng Li & Barry D. Bruce

  3. LABGeM, Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Université Evry, Université Paris-Saclay, Evry, France

    Alexandra Calteau

  4. Electron Microscopy Department, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Groningen, Netherlands

    Dmitry A. Semchonok & Egbert J. Boekema

  5. Collection of Cyanobacteria, Institut Pasteur, Paris, France

    Nathalie Sassoon & Muriel Gugger

  6. Pasarow Mass Spectrometry Laboratory, Geffen School of Medicine, University of California, Los Angeles, CA, USA

    Julian Whitelegge

  7. Microbiology Department, University of Tennessee, Knoxville, TN, USA

    Barry D. Bruce

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Contributions

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.

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Correspondence to Barry D. Bruce.

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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.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–10 and Supplementary Tables 1 and 2.

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Supplementary Data 1

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

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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). https://doi.org/10.1038/s41477-019-0566-x

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