, Volume 56, Issue 1, pp 294–299 | Cite as

Determination of PS I oligomerisation in various cyanobacterial strains and mutants by non-invasive methods

  • T. Zakar
  • L. Kovacs
  • S. Vajravel
  • E. Herman
  • M. Kis
  • H. Laczko-Dobos
  • Z. Gombos


PSI trimer to monomer ratio in intact cyanobacterial cells and isolated thylakoids was analysed by two noninvasive, in vivo methods; low-temperature fluorescence emission and circular dichroism spectroscopy. We measured fluorescence emission spectra of cells upon chlorophyll (Chl, 436 nm) excitation. All three species – Synechocystis sp. PCC 6803, Anabaena sp. PCC 7120, and Spirulina platensis – showed shifted Chl peak, indicating they have different spectral properties. CD spectroscopy revealed the highest intensity at 515 nm (PSI peak) in Spirulina platensis cells, which may originate from PSI multi-oligomerisation. The most sensitive response to heat treatment in this strain was the oligomerisation of PSI RCs. PSI dimers and tetramers in Anabaena cells showed smaller changes of the CD signal upon the heat treatment compared to that of Synechocystis WT. The lack of γ-linolenic acid affected the filament morphology by the loss of the spiral shape and the PSI monomerisation in Spirulina I22.

Additional key words

carotenoids pigment–protein interactions temperature stress xanthophylls 



Anabaena sp. PCC 7120








circular dichroism


xanthophyll- and PSI trimer-less mutant of Synechocystis sp. PCC 6803




γ-linolenic acid


γ-linolenic acid-deficient mutant of Spirulina platensis


long-wavelength chlorophyll






reaction center


ATCC Medium 1679


Spirulina platensis


Synechocystis sp. PCC 6803


wild type




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bautista J.A., Rappaport F., Guergova-Kuras M. et al.: Biochemical and biophysical characterization of photosystem I from phytoene desaturase and zeta-carotene desaturase deletion mutants of Synechocystis sp. PCC 6803: evidence for PsaA- and PsaB-side electron transport in cyanobacteria.–J. Biol. Chem. 280: 20030–20041, 2005.CrossRefPubMedGoogle Scholar
  2. Chitnis P.R.: Photosystem I.–Plant Physiol. 111: 661–669, 1996.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chitnis P.R.: Photosystem I: Function and Physiology.–Annu. Rev. Plant Phys. 52: 593–626, 2001.CrossRefGoogle Scholar
  4. Chitnis V.P., Chitnis P.R.: PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803.–FEBS Lett. 336: 330–334, 1993.CrossRefPubMedGoogle Scholar
  5. Chitnis V.P., Xu Q., Yu L., Golbeck J.H. et al.: Targeted inactivation of the gene psaL encoding a subunit of photosystem I of the cyanobacterium Synechocystis sp. PCC 6803.–J. Biol. Chem. 268: 11678–11684, 1993.PubMedGoogle Scholar
  6. Domonkos I., Kis M., Gombos Z. et al.: Carotenoids, versatile components of oxygenic photosynthesis.–Prog. Lipid Res. 52: 539–561, 2013.CrossRefPubMedGoogle Scholar
  7. El-Mohsnawy E., Kopczak M.J., Schlodder E. et al.: Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus.–Biochemistry 49: 4740–4751, 2010.CrossRefPubMedGoogle Scholar
  8. Fromme P., Jordan P., Krauss N.: Structure of photosystem I.–BBA-Bioenergetics 1507: 5–31, 2001.Google Scholar
  9. Garab G., van Amerongen H.: Linear dichroism and circular dichroism in photosynthesis research.–Photosynth. Res. 101: 135–146, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Gobets B., van Grondelle R.: Energy transfer and trapping in photosystem I.–Biochim. Biophys. Acta. 1507: 80–99, 2001.CrossRefPubMedGoogle Scholar
  11. Golbeck J.H.: Structure and function of Photosystem I.–Annu. Rev. Plant Phys. 43: 293–324, 1992.CrossRefGoogle Scholar
  12. Guskov A., Kern J., Gabdulkhakov A. et al.: Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride.–Nat. Struct. Mol. Biol. 16: 334–342, 2009.CrossRefPubMedGoogle Scholar
  13. Jordan P., Fromme P., Witt H.T. et al.: Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution.–Nature 411: 909–917, 2001.CrossRefPubMedGoogle Scholar
  14. Karapetyan N.V: Protective dissipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters.–Photosynth. Res. 97: 195–204, 2008.CrossRefPubMedGoogle Scholar
  15. Karapetyan N.V., Dorra D., Schweitzer G. et al.: Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis.–Biochemistry 36: 13830–13837, 1997.CrossRefPubMedGoogle Scholar
  16. Karapetyan N.V., Holzwarth A.R., Rogner M.: The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance.–FEBS Lett. 460: 395–400, 1999.CrossRefPubMedGoogle Scholar
  17. Kłodawska K., Kovács L., Várkonyi Z. et al.: Elevated growth temperature can enhance photosystem I trimer formation and affects xanthophyll biosynthesis in Cyanobacterium Synechocystis sp. PCC 6803 cells.–Plant Cell Physiol. 56: 558–571, 2015.CrossRefPubMedGoogle Scholar
  18. Komenda J., Barber J.: Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis.–Biochemistry 34: 9625–9631, 1995.CrossRefPubMedGoogle Scholar
  19. Kusama Y., Inoue S., Jimbo H. et al.: Zeaxanthin and Echinenone protect the repair of photosystem II from Inhibition by singlet oxygen in Synechocystis sp. PCC 6803.–Plant Cell Physiol. 56: 906–916, 2015.CrossRefPubMedGoogle Scholar
  20. Prentki P., Krisch M.H.: In vitro insertional mutagenesis with a selectable DNA fragment.–Gene 29: 303–313, 1984.CrossRefPubMedGoogle Scholar
  21. Rippka R., Deruelles J., Waterbury J. et al.: Generic assignments, strain histories and properties of pure cultures of cyanobacteria.–J. Gen. Microbiol. 111: 1–61, 1979.Google Scholar
  22. Schäfer L., Vioque A., Sandmann G.: Functional in situ evaluation of photosynthesis-protecting carotenoids in mutants of the cyanobacterium Synechocystis PCC 6803.–J. Photoch. Photobio. B 78: 195–201, 2005.CrossRefGoogle Scholar
  23. Schluchter W.M., Shen G., Zhao J. et al.: Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: a new model for state transitions in cyanobacteria.–Photochem. Photobiol. 64: 53–66, 1996.CrossRefPubMedGoogle Scholar
  24. Shubin V.V., Tsuprun V.L., Bezsmertnaya I.N. et al.: 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.CrossRefPubMedGoogle Scholar
  25. Sozer O., Komenda J., Ughy B. et al.: Involvement of carotenoids in the synthesis and assembly of protein subunits of photosynthetic reaction centers of Synechocystis sp. PCC 6803.–Plant Cell Physiol. 51: 823–835, 2010.CrossRefPubMedGoogle Scholar
  26. Takaichi S., Mochimaru M.: Carotenoids and carotenogenesis in cyanobacteria: unique ketocarotenoids and carotenoid glycosides.–Cell Mol. Life Sci. 64: 2607–2619, 2007.CrossRefPubMedGoogle Scholar
  27. Tian L., van Stokkum I.H., Koehorst R.B. et al.: Site, rate, and mechanism of photoprotective quenching in cyanobacteria.–J. Am. Chem. Soc. 133: 18304–18311, 2011.CrossRefPubMedGoogle Scholar
  28. Tóth T.N., Chukhutsina V., Domonkos I. et al.: Carotenoids are essential for the assembly of cyanobacterial photosynthetic complexes.–Biochim. Biophys. Acta. 1847: 1153–1165, 2015.CrossRefPubMedGoogle Scholar
  29. Trissl H.W.: Long-wavelength absorbing antenna pigments and heterogeneous absorption bands concentrate excitons and increase absorption cross section.–Photosynth. Res. 35: 247–263, 1993.CrossRefPubMedGoogle Scholar
  30. Turconi S., Kruip J., Schweitzer G. et al: A comparative fluorescence kinetics study of photosystem I monomers and trimers from Synechocystis PCC 6803.–Photosynth. Res. 49: 263–268, 1996.CrossRefPubMedGoogle Scholar
  31. Vajravel S., Kis M., Klodawska K. et al.: Zeaxanthin and echinenone modify the structure of photosystem I trimer in Synechocystis sp. PCC 6803.–BBA-Bioenergetics 1858: 510–518, 2017.CrossRefPubMedGoogle Scholar
  32. van Grondelle R., Dekker J.P., Gillbro T. et al.: Energy transfer and trapping in photosynthesis.–BBA-Bioenergetics 1187: 1–65, 1994.CrossRefGoogle Scholar
  33. Watanabe M., Semchonok D.A., Webber-Birungi M.T. et al.: Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria.–P. Natl. Acad. Sci. USA 111: 2512–2517, 2014.CrossRefGoogle Scholar
  34. Xu J., Ramian G.J., Galan J.F. et al.: Terahertz circular dichroism spectroscopy: a potential approach to the in situ detection of life’s metabolic and genetic machinery.–Astrobiology 3: 489–504, 2003.CrossRefPubMedGoogle Scholar
  35. Zakar T., Herman E., Vajravel S. et al.: Lipid and carotenoid cooperation-driven adaptation to light and temperature stress in Synechocystis sp. PCC 6803.–Biochim. Biophys. Acta 1858: 337–350, 2017.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • T. Zakar
    • 1
  • L. Kovacs
    • 1
  • S. Vajravel
    • 1
  • E. Herman
    • 1
  • M. Kis
    • 1
  • H. Laczko-Dobos
    • 1
  • Z. Gombos
    • 1
  1. 1.Institute of Plant Biology, Biological Research CentreHungarian Academy of SciencesSzegedHungary

Personalised recommendations