Advertisement

Hydroxyectoine protects Mn-depleted photosystem II against photoinhibition acting as a source of electrons

  • D. V. YanykinEmail author
  • M. Malferrari
  • S. Rapino
  • G. Venturoli
  • A. Yu Semenov
  • M. D. Mamedov
Original Article
First Online:
  • 38 Downloads

Abstract

In the present study, we have investigated the effect of hydroxyectoine (Ect-OH), a heterocyclic amino acid, on oxygen evolution in photosystem II (PS II) membrane fragments and on photoinhibition of Mn-depleted PS II (apo-WOC-PS II) preparations. The degree of photoinhibition of apo-WOC-PS II preparations was estimated by the loss of the capability of exogenous electron donor (sodium ascorbate) to restore the amplitude of light-induced changes of chlorophyll fluorescence yield (∆F). It was found that Ect-OH (i) stimulates the oxygen-evolving activity of PS II, (ii) accelerates the electron transfer from exogenous electron donors (K4[Fe(CN)6], DPC, TMPD, Fe2+, and Mn2+) to the reaction center of apo-WOC-PS II, (iii) enhances the protective effect of exogenous electron donors against donor-side photoinhibition of apo-WOC-PS II preparations. It is assumed that Ect-OH can serve as an artificial electron donor for apo-WOC-PS II, which does not directly interact with either the donor or acceptor side of the reaction center. We suggest that the protein conformation in the presence of Ect-OH, which affects the extent of hydration, becomes favorable for accepting electrons from exogenous donors. To our knowledge, this is the first study dealing with redox activity of Ect-OH towards photosynthetic pigment–protein complexes.

Keywords

Photosystem II Water-oxidizing complex Hydroxyectoine Photoinhibition 

Abbreviations

PS II

Photosystem II

RC

Reaction center

WOC

Water-oxidizing complex

apo-WOC-PS II

Photosystem II membrane fragments deprived of manganese

P680

The primary electron donor of PS II

QA, QB

The primary and secondary plastoquinone electron acceptor of PS II, respectively

PQ

Plastoquinone

PQH2

Plastoquinol

YZ

Redox-active tyrosine residue 161 of D1 protein

DPC

Diphenylcarbazide

TMPD

N,N,N′,N′-tetramethyl-p-phenylenediamine

MES

2-(N-morpholino)ethanesulfonic acid

Ect-OH

Hydroxyectoine ((4S,5S)-5-hydroxy-2-methyl-1,4,5,6-tetrahydropyrimidine-4-carboxylic acid)

ΔF

Photoinduced changes of chlorophyll fluorescence yield of PS II

Fo

The level of fluorescence induced by the measuring light

Fm

Maximal level of fluorescence

PI

Photoinhibition

This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

The authors would like to thank Dr. AA Khorobrykh for many useful comments and discussions. This work was supported by the RFBR № 17-00-00201. The results presented in Fig. 1 and Fig. S2 were obtained with support from the Russian Science Foundation (Grant 14-14-00535). The results presented in Fig. 4 were obtained with support from the Minobrnauki of Russia (theme AAAA-A17-117030110140-5).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2019_617_MOESM1_ESM.tif (4.2 mb)
Supplementary material 1 (TIF 4316 KB)
11120_2019_617_MOESM2_ESM.tif (617 kb)
Supplementary material 2 (TIF 617 KB)
11120_2019_617_MOESM3_ESM.tif (367 kb)
Supplementary material 3 (TIF 367 KB)
11120_2019_617_MOESM4_ESM.tif (1.2 mb)
Supplementary material 4 (TIF 1196 KB)
11120_2019_617_MOESM5_ESM.docx (18 kb)
Supplementary material 5 (DOCX 18 KB)

References

  1. Ablinger E, Hellweger M, Leitgeb S, Zimmer A (2012) Evaluating the effects of buffer conditions and extremolytes on thermostability of granulocyte colony-stimulating factor using high-throughput screening combined with design of experiments. Int J Pharm 436:744–752CrossRefGoogle Scholar
  2. Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition—a historical perspective. Photosynth Res 76:343–370CrossRefGoogle Scholar
  3. Allakhverdiev SI, Feyziev YM, Ahmed A, Hayashi H, Aliev JA, Klimov VV, Murata N, Carpentier R (1996) Stabilization of oxygen evolution and primary electron transport reactions in photosystem II against heat stress with glycinebetaine and sucrose. J Photochem Photobiol B 34(2–3):149–157CrossRefGoogle Scholar
  4. Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev JA, Klimov VV, Murata N, Carpentier R (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49CrossRefGoogle Scholar
  5. Allakhverdiev SI, Tomo T, Shimada Y, Kindo H, Nagao R, Klimov VV, Mimuro M (2010) Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc Natl Acad Sci USA 107:3924–3929CrossRefGoogle Scholar
  6. Allakhverdiev SI, Tsuchiya T, Watabe K, Kojima A, Los DA, Tomo T, Klimov VV, Mimuro M (2011) Redox potentials of primary electron acceptor quinone molecule (QA) and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc Natl Acad Sci USA 108:8054–8058CrossRefGoogle Scholar
  7. Ananev GM (1988) Effect of osmotic potential of the medium on oxygen evolution by pea thylakoids. Fiziologiya Rastenii 35:1115–1122Google Scholar
  8. Ananyev GM, Klimov VV (1988) Photoproduction bound hydrogen peroxide in subchloroplast preparations of photosystem II. Dokl AN SSSR (Russian) 298:1007–1011Google Scholar
  9. Ananyev G, Wydrzynski T, Renger G, Klimov V (1992) Transient peroxide formation by the manganese-containing redoxactive donor side of photosystem II upon inhibition of O2 evolution with lauroylcholine chloride. Biochim Biophys Acta 1100:303–311CrossRefGoogle Scholar
  10. Ananyev G, Renger G, Wacker U, Klimov V (1994) The photoproduction of superoxide radicals and the superoxide dismutase activity of Photosystem II. the possible involvement of cytochrome b559. Photosynth Res 41:327–338CrossRefGoogle Scholar
  11. Andersson MM, Breccia JD, Hatti-Kaul R (2000) Stabilizing effect of chemical additives against oxidation of lactate dehydrogenase. Biotechnol Appl Biochem 32:145–153CrossRefGoogle Scholar
  12. Apostolova E, Bushova M, Tenchov B (2005) Freezing damage and protective of photosystem 2 by sucrose and trehalose. In: Murata N (ed) Research photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 165–168Google Scholar
  13. Arakawa T, Timasheff SN (1985a) Mechanism of poly(ethylene glycol) interaction with proteins. Biochemistry 24(24):6756–6762CrossRefGoogle Scholar
  14. Arakawa T, Timasheff SN (1985b) The stabilization of proteins by osmolytes. Biophys J 47:411–414CrossRefGoogle Scholar
  15. Baranov SV, Tyryshkin AM, Katz D, Dismukes GC, Ananyev GM, Klimov VV (2004) Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex. Kinetics of reconstitution of O2 evolution by photoactivation. Biochemistry 43:2070–2079CrossRefGoogle Scholar
  16. Bard JS, Faulkner LR (2001) Electrochemical methods—fundamentals and Applications, 2nd edn. Wiley, New YorkGoogle Scholar
  17. Borges N, Ramos A, Raven NDH, Sharp RJ, Santos H (2002) Comparative study of the thermostabilizing properties of mannosylglycerate and other compatible solutes on model enzymes. Extremophiles 6:209–216CrossRefGoogle Scholar
  18. Brown AD, Rose AH, Morris JG (1978) Compatible solutes and extreme water stress in eukaryotic micro-organisms. In: Advances in microbial physiology. Academic Press, London, pp 181–242Google Scholar
  19. Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20CrossRefGoogle Scholar
  20. Czech L, Hermann L, Stöveken N, Richter AA, Höppner A, Smits SHJ, Heider J, Bremer E (2018) Role of the extremolytes ectoine and hydroxyectoine as stress protectants and nutrients: genetics, phylogenomics, biochemistry, and structural analysis. Genes 9:177CrossRefGoogle Scholar
  21. Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620CrossRefGoogle Scholar
  22. Ford RC, Evans MCW (1983) Isolation of a photosystem 2 preparation from higher plants with highly enriched oxygen evolution activity. FEBS Lett 160:159–164CrossRefGoogle Scholar
  23. Francia F, Palazzo G, Mallardi A, Cordone L, Venturoli G (2003) Residual water modulates QA – to QB electron transfer in bacterial reaction centers embedded in trehalose amorphous matrices. Biophys J 85(4):2760–2775CrossRefGoogle Scholar
  24. Galinski EA (1993) Compatible solutes of halophilic eubacteria: molecular principles, water–solute interaction, stress protection. Cell Mol Life Sci 49:487–496CrossRefGoogle Scholar
  25. Galinski EA, Pfeiffer HP, Truper HG (1985) 1,4,5,6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid: a novel cyclic amino acid from halophilic phototrophic bacteria of the genus Ectothiorhodospira. Eur J Biochem 149:135–139CrossRefGoogle Scholar
  26. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  27. Halverson KM, Barry BA (2003) Sucrose and glycerol effects on photosystem II. Biophys J 85:1317–1325CrossRefGoogle Scholar
  28. Harishchandra RK, Wulff S, Lentzen G, Neuhaus T, Galla H-J (2010) The effect of compatible solute ectoines on the structural organization of lipid monolayer and bilayer membranes. Biophys Chem 150:37–46CrossRefGoogle Scholar
  29. Haumann M, Hundelt M, Jahns P, Chroni S, Bogershausen O, Ghanotakis D, Junge W (1997) Proton release from water oxidation by photosystem II: similar stoichiometries are stabilized in thylakoids and PSII core particles by glycerol. FEBS Lett 410:243–248CrossRefGoogle Scholar
  30. Inbar L, Lapidot A (1988) The structure and biosynthesis of new tetrahydropyrimidine derivatives in actinomycin D producer Streptomyces parvulus. Use of 13C- and 15N-labeled L-glutamate and 13C and 15N NMR spectroscopy. J Biol Chem 263:16014–16022Google Scholar
  31. Ishikita H, Loll B, Biesiadka J, Saenger W, Knapp E-W (2005) Redox potentials of chlorophylls in the photosystem II reaction center. Biochemistry 44:4118–4124CrossRefGoogle Scholar
  32. Jegerschold C, Virgin I, Styring S (1990) Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry 29:6179–6186CrossRefGoogle Scholar
  33. Johnson GN, Rutherford AW, Krieger A (1995) A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution. Biochim Biophys Acta 1229:202–207CrossRefGoogle Scholar
  34. Khorobrykh SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynth Res 71:209–219CrossRefGoogle Scholar
  35. Khorobrykh AA, Klimov VV (2005) Effect of exogenous histidine on restoration of electron transfer on the donor side of photosystem II depleted of Mn. Photosynth Res 4(1–3):51–56CrossRefGoogle Scholar
  36. Khorobrykh AA, Klimov VV (2015) Involvement of molecular oxygen in the donor-side photoinhibition of Mn-depleted photosystem II membranes. Photosynth Res 126:417–425CrossRefGoogle Scholar
  37. Khorobrykh SA, Khorobrykh AA, Klimov VV, Ivanov BN (2002) Photoconsumption of oxygen in photosystem II preparations under impairment of the water-oxidizing complex. Biochemistry 67:683–688Google Scholar
  38. Khorobrykh SA, Khorobrykh AA, Yanykin DV, Ivanov BN, Klimov VV, Mano J (2011) Photoproduction of catalase-insensitive peroxides on the donor side of manganese-depleted photosystem II: evidence with a specific fluorescent probe. Biochemistry 50:10658–10665CrossRefGoogle Scholar
  39. Klimov VV, Allakhverdiev SI, Demeter S, Krasnovsky AA (1979) Photoreduction of pheophytin in chloroplast photosystem II as a function of the redox potential of the medium. Dokl AN SSSR (in Russian) 249:227–230Google Scholar
  40. Klimov VV, Allakhverdiev SI, Shuvalov VA, Krasnovsky AA (1982) Effect of extraction and re-addition of manganese on light reactions of photosystem II preparations. FEBS Lett 148:307–312CrossRefGoogle Scholar
  41. Klimov VV, Shafiev MA, Allakhverdiev SI (1990a) Photoinactivation of the reactivation capacity of photosystem II in pea subchloroplast particles after a complete removal of manganese. Photosynth Res 23:59–65CrossRefGoogle Scholar
  42. Klimov VV, Ananyev G, Allakhverdiev SI, Zharmukhamedov SK, Mulay M, Hegde U, Padhye S (1990b) Photoreactivation and photoinactivation of photosystem-II after a complete removal of manganese from pea subchloroplast particles. Curr Res Photosynth 1–4, A247–A254Google Scholar
  43. Klimov VV, Ananyev GM, Zastrizhnaya OM, Wydrzynski T, Renger G (1993) Photoproduction of hydrogen peroxide in photosystem II particles: a comparison of four signals. Photosynth Res 38:409–416CrossRefGoogle Scholar
  44. Klimov VV, Allakhverdiev SI, Nishiyama Y, Khorobrykh AA, Murata N (2003) Stabilization of the oxygen-evolving complex of photosystem II by bicarbonate and glycine betaine in thylakoid and subthylakoid preparations. Funct Plant Biol 30:797–803CrossRefGoogle Scholar
  45. Knapp S, Ladenstein R, Galinsky EA (1999) Extrinsic protein stabilization by the naturally occurring osmolytes ß-hydroxyectoine and betaine. Extremophiles 3:191–198CrossRefGoogle Scholar
  46. Kolp S, Pietsch M, Galinski EA, Gutschow M (2006) Compatible solutes as protectants for zymogens against proteolysis. Biochim Biophys Acta 1764:1234–1242CrossRefGoogle Scholar
  47. Krieger A, Weis E (1992) Energy-dependent quenching of chlorophyll-a-fluorescence: the involvement of proton-calcium exchange at photosystem 2. Photosynthetica 27:89–98Google Scholar
  48. Kruk J, Strzałka K (1999) Dark reoxidation of the plastoquinone-pool is mediated by the low potential form of cytochrome b559 in spinach thylakoids. Photosynth Res 62:273–279CrossRefGoogle Scholar
  49. Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: selective loss of quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 181:4070–4074CrossRefGoogle Scholar
  50. Lentzen G, Schwarz T (2006) Extremolytes: natural compounds from extremophiles for versatile applications. Appl Microbiol Biotechnol 72:623–634CrossRefGoogle Scholar
  51. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  52. Lippert K, Galinski EA (1992) Enzyme stabilization be ectoine-type compatible solutes: protection against heating, freezing and drying. Appl Microbiol Biotechnol 37:61–65CrossRefGoogle Scholar
  53. Malferrari M, Ghelli A, Roggiani F, Valenti G, Paolucci F, Rugolo M, Rapino S (2018) Reactive oxygen species produced by mutated mitochondrial respiratory chain of entire cells monitored with modified microelectrodes. ChemElectroChem.  https://doi.org/10.1002/celc.201801424 (In press)Google Scholar
  54. Mamedov MD, Hayashi H, Murata N (1993) Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron transport and phosphorylation reactions in Synechocystis PCC6803. Biochim Biophys Acta 1142:1–5CrossRefGoogle Scholar
  55. Mamedov MD, Hayashi H, Wada H, Mohanty PS, Papageorgiou GC, Murata N (1991) Glycinebetaine enhances and stabilizes the evolution of oxygen and the synthesis of ATP by cyanobacterial thylakoid membranes. FEBS Lett 294:271–274CrossRefGoogle Scholar
  56. Mamedov MD, Petrova OI, Yanykin DV, Zaspa AA, Semenov AY (2015) Effect of trehalose on oxygen evolution and electron transfer in photosystem 2 complexes. Biochemistry 80:61–66Google Scholar
  57. Mamedov MD, Nosikova ES, Vitukhnovskaya LA, Zaspa AA, Semenov AYu (2018) Influence of the disaccharide trehalose on the oxidizing side of photosystem II. Photosynthetica 56(1):236–243CrossRefGoogle Scholar
  58. McTavish H, Picorel R, Seibert M (1989) Stabilization of isolated photosystem II reaction center complex in the dark and in the light using polyethylene glycol and an oxygen-scrubbing system. Plant Physiol 89:452–456CrossRefGoogle Scholar
  59. Mohanty PS, Hayashi H, Papageorgiou GC, Murata N (1993) Stabilization of the Mn-cluster of the oxygen-evolving complex by glycinebetaine. Biochim Biophys Acta 1144:92–96CrossRefGoogle Scholar
  60. Nanba O, Satoh K (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84(1):109–112CrossRefGoogle Scholar
  61. Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99:481–485CrossRefGoogle Scholar
  62. Okamura MY, Satoh K, Isaacson RA, Feher G (1987) Evidence of the primary charge separation in the D1/D2 complex of photosystem 2 from spinach; EPR of the triplet state. Photosynth Res 1:379–381Google Scholar
  63. Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 44:243–252CrossRefGoogle Scholar
  64. Papageorgiou GC, Fujimura Y, Murata N (1991) Protection of the oxygen-evolving Photosystem ll complex by glycine betaine. Biochim Biophys Acta 1057:361–366CrossRefGoogle Scholar
  65. Pastor JM, Salvador M, Argandoña M, Bernal V, Reina-Bueno M, Csonka LN, Iborra JI, Vargas C, Nieto JJ, Cánovas M (2010) Ectoines in cell stress protection: uses and biotechnological production. Biotechnol Adv 28:782–801CrossRefGoogle Scholar
  66. Polander PC, Barry BA (2012) A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution. Proc Natl Acad Sci USA 109:6112–6117CrossRefGoogle Scholar
  67. Pospišil P, Šnyrychova I, Kruk J, Strzałka K, Nauš J (2006) Evidence that cytochrome b559 is involved in superoxide production in Photosystem II: effect of synthetic short-chain plastoquinones in a cytochrome b559 tobacco mutant. Biochem J 397:321–327CrossRefGoogle Scholar
  68. Pospísil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787:1151–1160CrossRefGoogle Scholar
  69. Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817:218–231CrossRefGoogle Scholar
  70. Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1(5):1–30.  https://doi.org/10.1186/1746-1448-1-5 Google Scholar
  71. Salmannejad F, Nafissi-Varcheh N (2017) Ectoine and hydroxyectoine inhibit thermal-induced aggreagation and oincrease thermostability of recombinant human interferon Alfa2b. Eur J Pharm Sci 97:200–207CrossRefGoogle Scholar
  72. Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen JR (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103CrossRefGoogle Scholar
  73. Tanaka A, Fukushima Y, Kamiya N (2017) Two different structures of the oxygen-evolving complex in the same polypeptide frameworks of photosystem II. J Am Chem Soc 139:1718–1721CrossRefGoogle Scholar
  74. Tanne C, Golovina EA, Hoekstra FA, Meffert A, Galinski EA (2014) Glass-forming property of hydroxyectoine is the cause of its superior function as a desiccation protectant. Front Microbiol 5(150):1–13.  https://doi.org/10.3389/fmicb.2014.00150 Google Scholar
  75. Tao P, Li H, Yu Y, Gu J, Liu Y (2016) Ectoine and 5-hydroxyectoine accumulation in the halophile Virgibacillus halodenitrificans PDB-F2 in response to salt stress. Appl Microbiol Biotechnol 100:6779–6789CrossRefGoogle Scholar
  76. Telfer A, Barber J, Evans M (1988) Oxidation-reduction potential dependence of reaction centre triplet formation in the isolated D1/D2 cytochrome b559 photosystem 2 complex. FEBS Lett 232:209–213CrossRefGoogle Scholar
  77. Telfer A, De Las Rivas J, Barber J (1991) b-carotene within the isolated photosystem II Reaction Centre: photooxidation and irreversible bleaching of this chromophore by oxidised P680. Biochim Biophys Acta 1060:106–114CrossRefGoogle Scholar
  78. Telfer A, Bishop SM, Phillips D, Barber J (1994) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J Biol Chem. 269:13244–13253Google Scholar
  79. Theg SM, Fillar LJ, Dilley RA (1986) Photoinactivation of chloroplasts already inhibited on the oxidizing side of photosystem II. Biochim Biphys Acta 849:104–111CrossRefGoogle Scholar
  80. Tyystjarvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303CrossRefGoogle Scholar
  81. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving Photosystem II at a resolution of 1.9 Å. Nature 473:55–61CrossRefGoogle Scholar
  82. Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:200–205CrossRefGoogle Scholar
  83. Williams WP, Gounaris K (1992) Stabilization of PS-II mediated electron transport in oxygen-evolving PS II core preparations by the addition of compatible co-solutes. Biochim Biophys Acta 1100:92–97CrossRefGoogle Scholar
  84. Williams WP, Brain APR, Dominy PJ (1992) Induction of non-bilayer lipid phase separations in chloroplast thylakoid membranes by compatible co-solutes and its relation to the thermal stability of Photosystem II. Biochim Biophys Acta 1099:137–144CrossRefGoogle Scholar
  85. Wydrzynski T, Angstrom J, Vanngard T (1989) H2O2 formation by photosystem II. Biochim Biophys Acta 973:23–28CrossRefGoogle Scholar
  86. Yanykin DV, Khorobrykh AA, Khorobrykh SA, Klimov VV (2010) Photoconsumption of molecular oxygen on both donor and acceptor sides of photosystem II in Mn-depleted subchloroplast membrane fragments. Biochim Biophys Acta 1797:516–523CrossRefGoogle Scholar
  87. Yanykin DV, Khorobrykh AA, Khorobrykh SA, Pshybytko NL, Klimov VV (2013) Flash-induced consumption of molecular oxygen on the donor side of photosystem II in Mn-depleted subchloroplast membrane fragments: specific effects of manganese and calcium ions. Photosynth Res 117:367–374CrossRefGoogle Scholar
  88. Yanykin DV, Khorobrykh AA, Zastrizhnaya OM, Klimov VV (2014) Interaction of molecular oxygen with the donor side of photosystem II after destruction of the water-oxidizing complex. Biochemistry 79:205–212Google Scholar
  89. Yanykin DV, Khorobrykh AA, Mamedov MD, Klimov VV (2015) Trehalose stimulation of photoinduced electron transfer and oxygen photoconsumption in Mn-depleted photosystem 2 membrane fragments. J Photochem Photobiol B 152:279–285CrossRefGoogle Scholar
  90. Yanykin DV, Khorobrykh AA, Mamedov MD, Klimov VV (2016) Trehalose protects Mn-depleted photosystem 2 preparations against the donor-side photoinhibition. J Photochem Photobiol B 164:236–243CrossRefGoogle Scholar
  91. Yanykin DV, Khorobrykh AA, Terentyev VV, Klimov VV (2017) Two pathways of photoproduction of organic hydroperoxides on the donor side of photosystem 2 in subchloroplast membrane fragments. Photosynth Res 133(1–3):129–138CrossRefGoogle Scholar
  92. Zaccai G, Bagyan I, Combet J, Cuello GJ, Deme B, Fichou Y, Gallat FX, Galvan Josa VM, von Gronau S, Haertlein M, Martel A, Moulin M, Neumann M, Weik M, Oesterhelt D (2016) Neutrons describe ectoine effects on water H-bonding and hydration around a soluble protein and a cell membrane. Sci Rep 6:31434. http://www.nature.com/articles/srep31434#article-comments

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute of Basic Biological Problems, FRC PSCBR RASPushchinoRussia
  2. 2.Department of Chemistry “Giacomo Ciamician”University of BolognaBolognaItaly
  3. 3.Laboratory of Biochemistry and Molecular Biophysics, Department of Pharmacy and Biotechnology, FaBiTUniversity of BolognaBolognaItaly
  4. 4.Belozersky Institute of Physical-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations

Cite article

Buy options