Photosynthetica 2018, 56(1):236-243 | DOI: 10.1007/s11099-017-0750-z

Influence of the disaccharide trehalose on the oxidizing side of photosystem II

M. D. Mamedov1,*, E. S. Nosikova2, L. A. Vitukhnovskaya1, A. A. Zaspa1, A. Yu. Semenov1
1 Belozersky Institute of Physical-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia
2 Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, Russia

The steady-state oxygen evolution rate was previously shown to be stimulated by the disaccharide trehalose in PSII suspension. Here we showed a similar increase in the rate of oxygen evolution in PSII core complexes from spinach in solution and in proteoliposomes in the presence of trehalose. Using direct electrometrical technique, we also revealed that trehalose had no effect on the kinetics of electron transfer from Mn to redox-active-tyrosyl radical, YZ* (S1 → S2 transition), while it accelerated the kinetics of electrogenic proton transport during S2 → S3 and S4 → S0 transitions of the wateroxidizing complex (WOC) induced by the first, second, and third laser flashes in dark-adapted PSII samples. These observations imply that the effect of trehalose occurrs due to its interaction with the WOC.

Keywords: effective functioning; osmolyte; photoelectric response; vectorial transfer

Received: April 26, 2017; Accepted: June 26, 2017; Published: March 1, 2018Show citation

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Mamedov, M.D., Nosikova, E.S., Vitukhnovskaya, L.A., Zaspa, A.A., & Yu. Semenov, A. (2018). Influence of the disaccharide trehalose on the oxidizing side of photosystem II. Photosynthetica56(1), 236-243. doi: 10.1007/s11099-017-0750-z.
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References

  1. Apostolova E., Bushova M., Tenchov B.: Thylakoid membranes during freeze-thaw treatment.-In: Murata N. (ed.): Research Photosynthesis, Vol. IV, Pp. 165-168, Kluwer Academic Publishers, Amsterdam 2005.
  2. Bakaltcheva I., Williams W.P., Schmitt J.M., Hincha D.K.: The solute permeability of thylakoid membranes is reduced by low concentrations of trehalose as a co-solute.-Biochim. Biophys. Acta 1189: 38-44, 1994. Go to original source...
  3. Carpenter J.F., Crowe J.H.: An infrared spectroscopic study of the interactions of carbohydrates with dried proteins.-Biochemistry 28: 3916-3922, 1989. Go to original source...
  4. Chang B., Yang L., Cong W. et al.: The improved resistance to high salinity induced by trehalose is associated with ionic regulation and osmotic adjustment in Catharanthus roseus.-Plant Physiol. Bioch. 77: 140-148, 2014. Go to original source...
  5. Conjeaud H., Mathis P.: The effect of pH on the reduction kinetics of P-680 in tris-treated chloroplasts.-BBABiochemistry 590: 353-359, 1980. Go to original source...
  6. Crowe J.H., Crowe L.M., Chapman D.: Preservation of membranes in anhydrobiotic organisms: the role of trehalose.-Science 223: 701-703, 1984. Go to original source...
  7. Crowe J.H., Crowe L.M., Oliver A.E. et al.: The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state.-Cryobiology 43: 89-105, 2001. Go to original source...
  8. Crowe J.H.: Anhydrobiosis: an unsolved problem.-Plant Cell Environ. 37: 1491-1493, 2014. Go to original source...
  9. Crowe L.M.: Lessons from nature: the role of sugars in anhydrobiosis.-Comp. Biochem. Phys. A 131: 505-513, 2002. Go to original source...
  10. Dau H., Haumann M.: Eight steps preceding O-O bond formation in oxygenic photosynthesis-a basic reaction cycle of the Photosystem II manganese complex.-BBA-Bioenergetics 1767: 472-483, 2007. Go to original source...
  11. de Wijn R., van Gorkom H.J.: The rate of charge recombination in Photosystem II.-BBA-Bioenergetics 1553: 302-308, 2002. Go to original source...
  12. Drachev L.A., Kaulen, A.D., Semenov A.Yu. et al.: Lipidimpregnated filters as a tool for studying the electric currentgenerating proteins.-Anal. Biochem. 96: 250-262, 1979. Go to original source...
  13. Fernandez O., Béthencourt L., Quero A. et al.: Trehalose and plant stress responses: friend or foe?-Trend. Plant Sci. 15: 409-417, 2010. Go to original source...
  14. Ferreira K.N., Iverson T.M., Maghlaoui K. et al.: Architecture of the photosynthetic oxygen-evolving center.-Science 303: 1831-1838, 2004. Go to original source...
  15. Ford R.C., Evans M.C.W.: Isolation of a photosystem 2 preparation from higher plants with highly enriched oxygen evolution activity.-FEBS Lett. 160: 159-164, 1983. Go to original source...
  16. Francia F., Malferrari M., Sacquin-Mora S., Venturoli G.: Charge recombination kinetics and protein dynamics in wild type and carotenoid-less bacterial reaction centers: studies in trehalose glasses.-J. Phys. Chem. 113: 10389-10398, 2009. Go to original source...
  17. Gerken S., Dekker J.P., Schlodder E., Witt H.T.: Studies on the multiphasic charge recombination between chlorophyll aII+ (P-680+) and plastoquinone QA- in photosystem II complexes. Ultraviolet difference spectrum of Chl-aII+/Chl-aII.-Biochim. Biophys. Acta 977: 52-61, 1989. Go to original source...
  18. Golub M., Hejazi M., Kölsch A. et al.: Solution structure of monomeric and trimeric Photosystem I of Thermosynechococcus elongatus investigated by small angle X-ray scattering.-Photosynth. Res., in press, Doi: 10.1007/s11120-017-0342-6, 2017. Go to original source...
  19. Gopta O.A., Tyunyatkina A.A., Kurashov V.N. et al.: Effect of redox mediators on the flash-induced membrane potential generation in Mn-depleted photosystem II core particles.-Eur. Biophys. J. 37: 1045-1050, 2008. Go to original source...
  20. Guskov A., Kern J., Gabdulkhakov A. et al.: Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride.-Nat. Struct. Mol. Biol. 16: 334-342, 2009.
  21. Haag E., Irrgang K.-D., Boekema E.J., Renger G.: Functional and structural analysis of photosystem II core complexes from spinach with high oxygen evolution capacity.-Eur. J. Biochem. 189: 47-53, 1990.
  22. Halverson K.M., Barry B.A.: Sucrose and glycerol effects on photosystem II.-Biophys. J. 85: 1317-1325, 2003. Go to original source...
  23. Harrigan P.R., Madden T.D., Cullis P.R.: Protection of liposomes during hydration and freezing.-Chem. Phys. Lipids 52: 139-149, 1990. Go to original source...
  24. Haumann M., Liebisch P., Müller C. et al.: Photosynthetic O2 formation tracked by time-resolved X-ray experiments.-Science 310: 1019-1021, 2005. Go to original source...
  25. Haumann M., Mulkidjanian A., Junge W.: Electrogenicity of electron and proton transfer at the oxidizing side of photosystem II.-Biochemistry 36: 9304-9315, 1997. Go to original source...
  26. Hincha D.K. Sieg F., Bakaltcheva I. et al.: Freeze-thaw damage to thylakoid membranes: specific protection by sugars and proteins.-In: Steponkus P.L. (ed.): Advances in Low-Temperature Biology, Vol. 3. Pp. 141-183, JAI Press, London 1996. Go to original source...
  27. Iturriaga G., Suárez R., Nova-Franco B.: Trehalose metabolism: from osmoprotection to signaling.-Int. J. Mol. Sci. 10: 3793-3810, 2009. Go to original source...
  28. Jain N.K., Roy I.: Effect of trehalose on protein structure.-Protein Sci. 18: 24-36, 2009
  29. Jun S.S., Yang J.Y., Choi H.J. et al.: Altered physiology in trehalose-producing transgenic tobacco plants: enhanced tolerance to drought and salinity stresses.-J. Plant Biol. 51: 327-336, 2008. Go to original source...
  30. Kalaidzidis Ya.L, Gavrilov A.V., Zaitsev P.V. et al: PLUK-an environment for software development.-Program Comput. Softw. 23: 206-212, 1997.
  31. Kan Z., Yan X., Ma J.: Conformation dynamics and polarization effect of α,α-trehalose in a vacuum and in aqueous and salt solutions.-J. Phys. Chem. A. 119: 1573-1589, 2015. Go to original source...
  32. Kawakami K., Umena Y., Kamiya N., Shen J.-R.: Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution.-J. Photoch. Photobio. B 104: 9-18, 2011. Go to original source...
  33. Kok B., Forbush B., McGloin M.: Cooperation of charges in photosynthetic O2 evolution. I. A linear four-step mechanism.-Photochem. Photobiol. 11: 457-475, 1970. Go to original source...
  34. Lunn J.E., Delorge I., Figueroa C.M. et al.: Trehalose metabolism in plants.-Plant J. 79: 544-567, 2014. Go to original source...
  35. Luo Y., Li F., Wang G.P. et al.: Exogenously-supplied trehalose protects thylakoid membranes of winter wheat from heatinduced damage.-Biol. Plantarum 54: 495-501, 2010. Go to original source...
  36. Malferrari M., Nalepa A., Venturoli G. et al.: Structural and dynamical characteristics of trehalose and sucrose matrices at different hydration levels as probed by FTIR and high-field EPR.-Phys. Chem. Chem. Phys. 16: 9831-9848, 2014. Go to original source...
  37. Malferrari M., Savitsky A., Lubitz W. et al.: Protein immobilization capabilities of sucrose and trehalose glasses: the effect of protein/sugar concentration unraveled by high-field EPR.-J. Phys. Chem. Lett. 7: 4871-4877, 2016. Go to original source...
  38. Mamedov M.D., Beshta O.E., Gurovskaya K.N. et al.: Photoelectric responses of oxygen-evolving complexes of photosystem II.-Biochemistry-Moscow+ 64: 606-611, 1999.
  39. Mamedov M.D., Kurashov V.N., Cherepanov D.A., Semenov A.Yu.: Photosystem II: Where does the light-induced voltage come from?-Front. Biosci. 15: 1007-1017, 2010.
  40. Mamedov M.D., Petrova I.O., Yanykin D.V. et al.: Effect of trehalose on oxygen evolution and electron transfer in photosystem 2 complexes.-Biochemistry-Moscow+ 80: 61-66, 2015. Go to original source...
  41. Mamedov M.D., Tyunyatkina A.A., Siletsky S.A., Semenov A.Yu.: Voltage changes involving photosystem II quinone-iron complex turnover.-Eur. Biophys. J. 35: 647-654, 2006. Go to original source...
  42. McEvoy J.P., Brudvig G.W.: Redox reactions of the non-heme iron in photosystem II: An EPR spectroscopic study.-Biochemistry 47: 13394-13403, 2008. Go to original source...
  43. Muh F., Zouni A.: Light-induced water oxidation in photosystem II.-Front. Biosci. 16: 3072-3132, 2011. Go to original source...
  44. Najafpour M.M., Renger G., Hołyńska M. et al.: Manganese compounds as water-oxidizing catalysts: From the natural water-oxidizing complex to nanosized manganese oxide structures.-Chem. Rev. 116: 2886-2936, 2016. Go to original source...
  45. Noguchi T., Sugiura M.: Flash-induced FTIR difference spectra of the water-oxidizing complex in moderately hydrated photosystem II core films: Effect of hydration extent on S-state transitions.-Biochemistry 41: 2322-2330, 2002. Go to original source...
  46. Ohtake S., Wang Y.J.: Trehalose: current use and future applications.-J. Pharm. Sci. 100: 2020-2053, 2011. Go to original source...
  47. Palazzo G., Francia F., Mallardi A. et al.: Water activity regulates the QA- to QB electron transfer in photosynthetic reaction centers from Rhodobacter sphaeroides.-J. Am. Chem. Soc. 130: 9353-9363, 2008. Go to original source...
  48. Petrova I.O., Kurashov V.N., Zaspa A.A. et al.: Vectorial charge transfer reactions on the donor side of manganese-depleted and reconstituted photosystem 2 core complexes.-Biochemistry-Moscow+ 78: 395-402, 2013. Go to original source...
  49. Polander P.C., Barry B.A.: A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution.-P. Natl. Acad. Sci. USA 109: 6112-6117, 2012. Go to original source...
  50. Renger G., Kühn P.: Reaction pattern and mechanism of light induced oxidative water splitting in photosynthesis.-BBABioenergetics 1767: 458-471, 2007. Go to original source...
  51. Semenov A., Cherepanov D., Mamedov M.: Electrogenic reactions and dielectric properties of photosystem II.-Photosynth. Res. 98: 121-130, 2008. Go to original source...
  52. Semenov A.Y., Mamedov M.D., Chamorovsky S.K.: Electrogenic reactions associated with electron transfer in photosystem I.-In: Golbeck J.H. (ed.): Advances in Photosynthesis and Respiration Series. Photosystem I: the Light-driven, Platocyanin:Ferredoxin Oxidoreductase. Chapter 21. Pp. 319-424. Springer, Dordrecht 2006. Go to original source...
  53. Shevela D., Eaton-Rye J.J., Shen J.R., Govindjee.: Photosystem II and the unique role of bicarbonate: a historical perspective.-Biochim. Biophys. Acta. 1817: 1134-1151, 2012.
  54. Shimada Y., Suzuki H., Tsuchiya T. et al.: Structural coupling of an arginine side chain with the oxygen-evolving Mn4Ca cluster in photosystem II as revealed by isotope-edited Fourier transform infrared spectroscopy.-J. Am. Chem. Soc. 133: 3808-3811, 2011.
  55. Shinkarev V.P., Wraight C.A.: Oxygen evolution in photosynthesis: from unicycle to bicycle.-P. Natl. Acad. Sci. USA 90: 1834-1838, 1993.
  56. Shinkarev V.P.: Photosystem II: Oxygen evolution and chlorophyll a fluorescence induced by multiple flashes.-In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll Fluorescence: a Signature of Photosynthesis. Pp. 197-229. Kluwer Academic Publishers, Amsterdam 2
  57. Shoji M., Isobe H., Yamanak S. et al.: Theoretical insight in to hydrogen-bonding networks and proton wire for the CaMn4O5 cluster of photosystem II. Elongation of Mn-Mn distances with hydrogen bonds.-Catal. Sci. Technol. 3: 1831-1848, 2013.
  58. Shutova T., Klimov V.V., Andersson B., Samuelsson G.A.: Cluster of carboxylic groups in PsbO protein is involved in proton transfer from the water oxidizing complex of photosystem II.-BBA-Bioenergetics 1767: 434-440, 2007. Go to original source...
  59. Umena Y., Kawakami K., Shen J.-R., Kamiya N.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.-Nature 473: 55-60, 2011. Go to original source...
  60. Uribe S., Sampedro J.G.: Measuring solution viscosity and its effect on enzyme activity.-Biol. Proced. Online. 5: 108-115, 2003. Go to original source...
  61. Villarreal M.A., Díaz S.B., Disalvo E.A., Montich G.C.: Molecular dynamics simulation study of the interaction of trehalose with lipid membranes.-Langmuir 20: 7844-7851, 2004. Go to original source...
  62. Vinyard D.J., Brudvig G.W.: Progress toward a molecular mechanism of water oxidation in photosystem II.-Annu. Rev. Phys. Chem. 68: 101-116, 2017. Go to original source...
  63. Williams W.P., Brain A.P.R., Dominy P.J.: Induction of nonbilayer lipid phase separations in chloroplast thylakoid membranes by compatible co-solutes and its relation to the thermal stability of Photosystem II.-Biochim. Biophys. Acta 1099: 137-144, 1992.
  64. Williams W.P., Gounaris K.: Stabilization of PS-II mediated electron transport in oxygen-evolving PS II core preparations by the addition of compatible co-solutes.-Biochim. Biophys. Acta 1100: 92-97, 1992. Go to original source...
  65. Wydrzynski T.J., Satoh K.: Photosystem II: The Light-driven Water:Plastoquinone Oxidoreductase. Pp. 11-22. Springer, New York 2005.
  66. Yanykin D.V., Khorobrykh A.A., Mamedov M.D., Klimov V.V.: Trehalose stimulation of photoinduced electron transfer and oxygen photoconsumption in Mn-depleted photosystem 2 membrane fragments.-J. Photoch. Photobio. B. 152(Pt B): 279-285, 2015. Go to original source...
  67. Yanykin D.V., Khorobrykh A.A., Mamedov M.D., Klimov V.V.: Trehalose protects Mn-depleted photosystem 2 preparations against the donor-side photoinhibition.-J. Photoch. Photobio. B. 164: 236-243, 2016. Go to original source...