Response of Synechocystis sp. PCC 6803 to UV radiations by alteration of polyamines associated with thylakoid membrane proteins

  • Suparaporn Khanthasuwan
  • Aran Incharoensakdi
  • Saowarath JantaroEmail author
Original Paper


The responses of Synechocystis sp. PCC 6803 exposed to UVA, UVB and UVC for at least 3 h were investigated with the emphasis on the changes of polyamines (PAs) levels in whole cells, thylakoid membrane fraction, and thylakoid membrane-associated proteins fraction. All UV radiations caused a slight decrease on cell growth but a drastic reduction of photosynthetic efficiency of Synechocystis cells. UV radiations, especially UVB and UVC, severely decreased the levels of PAs associated with thylakoid membrane proteins. The decreased PAs levels as affected by UV radiation correlated well with the decrease of photosynthetic efficiency, suggesting the role of PAs for the maintenance of photosynthetic activity of Synechocystis. PAs, especially spermidine (Spd) and putrescine (Put), were found abundantly in the thylakoid membrane fraction, and these PAs were associated mainly with the PSI trimer complex. Importantly, the exposure of Synechocystis cells to all UV radiations for 3 h resulted in the increase of Spd associated with the PSII monomer and dimer complex, suggesting its protective role against UV radiations despite the overall decrease of PAs.

Graphical abstract


Thylakoid membrane protein complexes Polyamine association, Synechocystis sp. PCC 6803 Stress response UV radiations 





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This work was supported by the Scholarship from the Graduate School, Chulalongkorn University to commemorate the 72nd anniversary of his Majesty King Bhumibala Aduladeja and the 90th Anniversary Chulalongkorn University Fund (Ratchadaphisekspmphot Endowment Fund) to S.K.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317CrossRefGoogle Scholar
  2. Barbato R, Bergo E, Szabò I, Vecchia FD, Giacometti GM (2000) Ultraviolet B exposure of whole leaves of barley affects structure and functional organization of photosystem II. J Biol Chem 275:10976–10982CrossRefGoogle Scholar
  3. Beauchemin R, Harmois J, Rouillon R, Tajmir-Riahi HA, Carpentier R (2007) Interaction of polyamines with protein of photosystem II: cation binding and photosynthetic oxygen evolution. J Mol Struct 833:169–174CrossRefGoogle Scholar
  4. Bebout BM, Garcia-Pichel F (1995) UV-B induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61:4215–4222PubMedPubMedCentralGoogle Scholar
  5. Bird RE, Hulstrom RL, Lewis LJ (1983) Terrestrial solar spectral data sets. Sol Energy 30:563–573CrossRefGoogle Scholar
  6. Bograh A, Gingras Y, Tajmir-Riahi HA, Carpentier R (1997) The effects of spermine and spermidine on the structure of photosystem II proteins in relation to inhibition of electron transport. FEBS Lett 402:41–44CrossRefGoogle Scholar
  7. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  9. Burton DR, Forsén S, Reimarsson P (1981) The interaction of polyamines with DNA: a 23Na NMR study. Nucleic Acids Res 9:1219–1228CrossRefGoogle Scholar
  10. Chamovitz D, Sandmann G, Hirschberg J (1993) Molecular and biochemical characterization of herbicide-resistant mutants of cyanobacteria reveals that phytoene desaturation is a rate-limiting step in carotenoid biosynthesis. J Biol Chem 268:17348–17353PubMedGoogle Scholar
  11. D’Orazio J, Jarrett S, Amaro-Ortiz A, Scott T (2013) UV radiation and the skin. Int J Mol Sci 14:12222–12248CrossRefGoogle Scholar
  12. Daddy S, Zhan J, Jantaro S, He C, He Q, Wang Q (2015) A novel high light-inducible carotenoid-binding protein complex in the thylakoid membranes of Synechocystis PCC 6803. Sci Rep 5:9480CrossRefGoogle Scholar
  13. Ehling-Schulz M, Scherer S (1999) UV protection in cyanobacteria. Eur J Phycol 34:329–338CrossRefGoogle Scholar
  14. Farman JC, Gardiner BG, Shanklin JD (1985) Large losses of total ozone in Antractica reveal seasonal ClOx/NOx interaction. Nature 315:207–210CrossRefGoogle Scholar
  15. Feuerstein BG, Pattabiraman N, Marton LJ (1986) Spermine-DNA interactions: a theoretical study. Proc Natl Acad Sci USA 83:5948–5952CrossRefGoogle Scholar
  16. Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant D (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317CrossRefGoogle Scholar
  17. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45CrossRefGoogle Scholar
  18. Hamdani S, Yaakoubi H, Carpentier R (2011) Polyamines interaction with thylakoid proteins during stress. ‎J Photochem Photobiol B 104:314–319CrossRefGoogle Scholar
  19. He YY, Häder D (2002) Reactive oxygen species and UV-B: effect on cyanobacteria. Photochem Photobiol Sci 1:729–736CrossRefGoogle Scholar
  20. Ioannidis NE, Kotzabasis K (2007) Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta 1767:1372–1382CrossRefGoogle Scholar
  21. Ioannidis NE, Sfichi L, Kotzabasis K (2006) Putrescine stimulates chemiosmotic ATP synthesis. Biochim Biophys Acta 1757:821–828CrossRefGoogle Scholar
  22. Jantaro S, Mäenpää P, Mulo P, Incharoensakdi A (2003) Content and biosynthesis of polyamines in salt and osmotically-stressed cells of Synechocystis sp. PCC 6803. FEMS Microbiol Lett 228:129–135CrossRefGoogle Scholar
  23. Jantaro S, Ali Q, Lone S, He Q (2006) Suppression of lethality of high light to a quadruple HLI mutant by the inactivation of the regulatory protein PfsR in Synechocystis PCC 6803. J Biol Chem 281:30865–30874CrossRefGoogle Scholar
  24. Jantaro S, Pothipongsa A, Khanthasuwan S, Incharoensakdi A (2011) Short-term UV-B and UV-C radiations preferentially decrease spermidine contents and arginine decarboxylase transcript levels of Synechocystis sp. PCC 6803. Curr Microbiol 62:420–426CrossRefGoogle Scholar
  25. Jantaro S, Baebprasert W, Piyamawadee C, Sodsuay O, Incharoensakedi A (2014) Exogenous spermidine alleviated UV-induced growth inhibition of Synechocystis sp. PCC 6803 via reduction of hydrogen peroxide and malonaldehyde levels. Appl Biochem Biotechnol 173:1145–1156CrossRefGoogle Scholar
  26. Kootstra A (1994) Protection from UV-B-induced DNA damage by flavonoids. Plant Mol Biol 26:771–774CrossRefGoogle Scholar
  27. Kotzabasis K, Fotinou C, Roubelakis-Angelakis KA, Ghanotakis D (1993) Polyamines in the photosynthetic apparatus. Photosystem II highly resolved subcomplexes are enriched in spermine. Photosynth Res 38:83–88CrossRefGoogle Scholar
  28. Kotzabasis K, Navakoudis E, Tsolakis G, Senger H, Dörnemann D (1999) Characterization of the photoreceptor(s) responsible for the regulation of the intracellular polyamine level and the putative participation of heterotrimeric G-proteins in the signal transduction chain. J Photochem Photobiol B 50:38–44CrossRefGoogle Scholar
  29. Lütz C, Navakoudis E, Seidlitz HK, Kotzabasis K (2005) Simulated solar irradiation with enhanced UV-B adjust plastid- and thylakoid-associated polyamine changes for UV-B protection. ‎Biochim Biophys Acta 1710:24–33CrossRefGoogle Scholar
  30. Matsui K, Nazifi E, Hirai Y, Wada N, Matsugo S, Sakamoto T (2012) The cyanobacterial UV-absorbing pigment scytonemin displays radical scavenging activity. J Gen Appl Microbiol 58:137–144CrossRefGoogle Scholar
  31. Moran R (1982) Formulae for determination of chlorophyllous pigments extracted with N, N-dimethylformamide. Plant Physiol 69:1376–1381CrossRefGoogle Scholar
  32. Navakoudis E, Lütz C, Langebartels C, Lütz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. ‎Biochim Biophys Acta-Bioenergetics 1621:160–169CrossRefGoogle Scholar
  33. Rastogi RP, Incharoensakdi A (2014) Characterization of UV-screening compounds, mycosporine-like amino acids, and scytonemin in the cyanobacterium Lyngbya sp. CU2555. FEMS Microbiol Ecol 87:244–256CrossRefGoogle Scholar
  34. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stainer RY (1979) Generic assignment, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  35. Sfakianaki M, Sfichi S, Kotzabasis K (2006) The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature. J Photochem Photobiol B 84:181–188CrossRefGoogle Scholar
  36. Shu S, Guo S-R, Yuan L-Y (2012) A review: polyamines and photosynthesis. In: Najafpour M (ed) Advances in photosynthesis—fundamental aspects. InTech Open, London. ISBN: 978-953-307-928-8Google Scholar
  37. Stapleton AE, Walbot V (1994) Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiol 105:881–889CrossRefGoogle Scholar
  38. Wang Q, Jantaro S, Bingshe L, Majeed W, Bailey M, He Q (2008) The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol 147:1239–1250CrossRefGoogle Scholar
  39. Xue L, Zhang Y, Zhang T, An L, Wang X (2005) Effects of enhanced ultraviolet-B radiation on algae and cyanobacteria. Crit Rev Microbiol 31:79–89CrossRefGoogle Scholar
  40. Yaakoubi H, Hasni I, Tajmir-Riahi HA, Carpentier R (2014) Effect of biogenic polyamine spermine on the structure and function of photosystem I. J Photochem Photobiol B: Biol 141:76–83CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Program in Biotechnology, Faculty of ScienceChulalongkorn UniversityBangkokThailand
  2. 2.Laboratory of Cyanobacterial Biotechnology, Department of Biochemistry, Faculty of ScienceChulalongkorn UniversityBangkokThailand

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