Photosynthesis Research

, Volume 139, Issue 1–3, pp 295–305 | Cite as

Hybrid complexes of photosynthetic reaction centers and quantum dots in various matrices: resistance to UV irradiation and heating

  • Peter P. Knox
  • Evgeny P. Lukashev
  • Vladimir V. Gorokhov
  • Nadezhda P. Grishanova
  • Vladimir Z. PaschenkoEmail author
Original Article


The effects of ultraviolet (UV) irradiation (up to 0.6 J/cm2) and heating (65 °C, 20 min) on the absorption spectra and electron transfer in dehydrated film samples of photosynthetic reaction centers (RCs) from purple bacterium Rhodobacter (Rb.) sphaeroides, as well as in hybrid structures consisting of RCs and quantum dots (QDs), have been studied. The samples were placed in organic matrices containing the stabilizers of protein structure—polyvinyl alcohol (PVA) and trehalose. UV irradiation led to partially irreversible oxidation of some RCs, as well as to transformation of some fraction of the bacteriochlorophyll (BChl) molecules into bacteriopheophytin (BPheo) molecules. In addition, UV irradiation causes degradation of some BChl molecules that is accompanied by formation of 3-acetyl-chlorophyll a molecules. Finally, UV irradiation destroys the RCs carotenoid molecules. The incorporation of RCs into organic matrices reduced pheophytinization. Trehalose was especially efficient in reducing the damage to the carotenoid and BChl molecules caused by UV irradiation. Hybrid films containing RC + QD were more stable to pheophytinization upon UV irradiation. However, the presence of QDs in films did not affect the processes of carotenoid destruction. The efficiency of the electronic excitation energy transfer from QD to P865 also did not change under UV irradiation. Heating led to dramatic destruction of the RCs structure and bacteriochlorins acquired the properties of unbound molecules. Trehalose provided strong protection against destruction of the RCs and hybrid (RC + QD) complexes.


Photosynthetic reaction centers Quantum dots Organic matrices PVA Trehalose Heating UV irradiation Hybrid complexes stability 



Reaction center


Quantum dot






Photoactive dimer of BChl




Polyvinyl alcohol


Photooxidized dimer of BChl

QA and QB

Primary and secondary quinone acceptors

Rb. sphaeroides

Purple bacteria Rhodobacter sphaeroides



This study was supported by the Russian Foundation for Basic Research (Project No. 15-29-01167).


  1. 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
  2. Čejková J, Čejka Č, Ardan T, Širc J, Michálek J, Luyckx J (2010) Reduced UVB-induced corneal damage caused by reactive oxygen and nitrogen species and decreased changes in corneal optics after trehalose treatment. Histol Histopathol 25:1403–1416Google Scholar
  3. Chen G, Djuric Z (2001) Carotenoids are degraded by free radicals but do not affect lipid peroxidation in unilamellar liposomes under different oxygen tensions. FEBS Lett 505:151–154CrossRefGoogle Scholar
  4. Chen X, Li M, Li L, Xu S, Huang D, Ju M, Huang Y, Chen K, Gu H (2016) Trehalose, sucrose and raffinose are novel activators of autophagy in human keratinocytes through an mTOR-independent pathway. Sci Rep 6:28423CrossRefGoogle Scholar
  5. Clayton RK (1978) Effects of dehydration on reaction centers from Rps. sphaeroides. Biochim Biophys Acta 504:255–264CrossRefGoogle Scholar
  6. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599CrossRefGoogle Scholar
  7. D’Alfonso L, Collini M, Cannone F, Chirico G, Campanini B, Cottone G, Cordone L (2007) GFP-mut2 proteins in trehalose-water matrixes: spatially heterogeneous protein-water-sugar structures. Biophys J 93:284–293CrossRefGoogle Scholar
  8. De Las Rivas J, Barber J (1997) Structure and thermal stability of photosystem II reaction centers studied by infrared spectroscopy. Biochemistry 36:8897–8903CrossRefGoogle Scholar
  9. Francia F, Palazzo G, Mallardic A, Cordoned L, Venturoli G (2004) Probing light-induced conformational transitions in bacterial photosynthetic reaction centers embedded in trehalose–water amorphous matrices. Biochim Biophys Acta 1658:50–57CrossRefGoogle Scholar
  10. Gast P, Hemelrijk PW, Van Gorkom HJ, Hoff AJ (1996) The association of different detergents with the photosynthetic reaction center protein of Rhodobacter sphaeroides R26 and the effects on its photochemistry. Eur J Biochem 239:805–809CrossRefGoogle Scholar
  11. Gingras G (1978) A comparative review of photochemical reaction center preparations from photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 119–131Google Scholar
  12. Giuffrida S, Cottone G, Cordone L (2004) Structure—dynamics coupling between protein and external matrix in sucrose-coated and in trehalose-coated MbCO: an FTIR study. J Phys Chem B 108:15415–15421CrossRefGoogle Scholar
  13. Hughes AV, Rees P, Heathcote P, Jones MR (2006) Kinetic analysis of the thermal stability of the photosynthetic reaction center from Rhodobacter sphaeroides. Biophys J 90:4155–4166CrossRefGoogle Scholar
  14. Ivanov AG, Miskiewicz E, Clarke AK, Greenberg BM, Huner NPA (2000) Protection of photosystem II against UV-A and UV-B-radiation in the cyanobacterium Plectonema boryanum: the role of growth temperature and growth irradiance. Photochem Photobiol 72:772–779CrossRefGoogle Scholar
  15. Karpulevich AA, Maksimov EG, Sluchanko NN, Vasiliev AN, Paschenko VZ (2016) Highly efficient energy transfer from quantum dot to allophycocyanin in hybrid structures. J Photochem Photobiol B 160:96–101CrossRefGoogle Scholar
  16. Karpulevich AA, Maksimov EG, Gorokhov VV, Churin AA, Ivanov MV, Paschenko VZ (2017) Covalently linked hybrid structures of semiconductor nanocrystals and allophycocyanin. Nanotechnol Russ 12:98–106CrossRefGoogle Scholar
  17. Knox PP, Kononenko AA, Rubin AB (1979) Functional activity in photosynthetic reaction centers from Rhodopseudomonas sphaeroides at fixed hydration levels of the preparations. Bioorganic Chem (USSR) 5:879–885Google Scholar
  18. Knox PP, Lukashev EP, Timofeev KN, Seifullina NK (2002) Effects of oxygen on the dark recombination between photoreduced secondary quinone and oxidized bacteriochlorophyll in Rhodobacter sphaeroides reaction centers. Biochemistry 67:901–907Google Scholar
  19. Konov KB, Isaev NP, Dzuba SA (2014) Low-temperature molecular motions in lipid bilayers in the presence of sugars: insights into cryoprotective mechanisms. J Phys Chem B 118:12478–12485CrossRefGoogle Scholar
  20. Kotakis C, Akhtar P, Zsiros O, Garab G, Lambrey PH (2018) Increased thermal stability of photosystem II and the macro-organization of thylakoid membranes, induced by co-solutes, associated with changes in the lipid-phase behaviour of thylakoid membranes. Photosynthetica 56:254–264CrossRefGoogle Scholar
  21. Lancaster CRD, Michel H, Honig B, Gunner MR (1996) Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis. Biophys J 70:2469–2492CrossRefGoogle Scholar
  22. Leatherdale CA, Woo WK, Mikulec FV, Bawendi MG (2002) On the absorption cross section of CdSe nanocrystal quantum dots. J Phys Chem B 106:7619–7622CrossRefGoogle Scholar
  23. Lukashev EP, Knox PP, Gorokhov VV, Grishanova NP, Seifullina NK, Krikunova M, Lokstein H, Paschenko VZ (2016a) Purple bacterial photosynthetic reaction centers and quantum-dot hybrid-assemblies in lecithin liposomes and thin films. J Photochem Photobiol B 164:73–82CrossRefGoogle Scholar
  24. Lukashev EP, Knox PP, Oleinikov IP, Seifullina NK, Grishanova NP (2016b) Investigation of stability of photosynthetic reaction center and quantum dot hybrid films. Biochemistry 81:58–63Google Scholar
  25. Makhneva ZK, Ashikhmin AA, Bolshakov MA, Moskalenko AA (2016) 3-Acetyl-chlorophyll formation in light-harvesting complexes of purple bacteria by chemical oxidation. Biochemistry 81:176–186Google Scholar
  26. Maksimov EG, Gostev TS, Kuz’minov FI, Sluchanko NN, Stadnichuk IN, Pashchenko VZ, Rubin AB (2010) Hybrid systems of quantum dots mixed with the photosensitive protein phycoerythrin. Nanotechnol Russ 5:531–537CrossRefGoogle Scholar
  27. Malferrari M, Savitsky A, Mamedov MD, Milanovsky GE, Lubitz W, Möbius K, Semenov AY, Venturoli G (2016) Trehalose matrix effects on charge-recombination kinetics in рhotosystem I of oxygenic photosynthesis at different dehydration levels. Biochim Biophys Acta 1857:1440–1454CrossRefGoogle Scholar
  28. McConnell I, Li G, Brudvig GW (2010) Energy conversion in natural and artificial photosynthesis. Chem Biol 17:434–447CrossRefGoogle Scholar
  29. Miksovska J, Maroti P, Tandori J, Schiffer M, Hanson DK, Sebban P (1996) Distant electrostatic interactions modulate the free energy level of QA in the photosynthetic reaction center. Biochemistry 35:15411–15417CrossRefGoogle Scholar
  30. Nabiev I, Rakovich A, Sukhanova A, Lukashev E, Zagidullin V, Paschenko V, Rakovich Y, Donegan J, Rubin A, Govorov A (2010) Fluorescent quantum dots as artificial antennas for enhanced light harvesting and energy transfer to photosynthetic reaction centers. Angew Chem Int Ed 49:7217–7221CrossRefGoogle Scholar
  31. Okamura MY, Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61:861–896CrossRefGoogle Scholar
  32. Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458:148–163CrossRefGoogle Scholar
  33. Oleynikov VA, Sukhanova AV, Nabiev IR (2007) Fluorescent semiconductor nanocrystals for biology and medicine. Russ Nanotechnol 2:160–173Google Scholar
  34. Olsson C, Jansson H, Swenson J (2016) The role of trehalose for the stabilization of proteins. J Phys Chem B 120:4723–4731CrossRefGoogle Scholar
  35. Ormerod JG, Ormerod KS, Gest H (1961) Dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; Relationships with nitrogen metabolism. Arch Biochem Biophys 94:449–463CrossRefGoogle Scholar
  36. Palazzo G, Mallardi A, Hochkoeppler A, Cordone L, Venturoli G (2002) Electron transfer kinetics in photosynthetic reaction centers embedded in trehalose glasses: trapping of conformational substates at room temperature. Biophys J 82:558–568CrossRefGoogle Scholar
  37. Rabenstein B, Ullmann GM, Knapp EW (2000) Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes. Biochemistry 39:10487–10496CrossRefGoogle Scholar
  38. Razjivin AP, Lukashev EP, Kompanets VO, Kozlovsky VS, Ashikhmin AA, Chekalin SV, Moskalenko AA, Paschenko VZ (2017) Excitation energy transfer from the bacteriochlorophyll Soret band to carotenoids in the LH2 light-harvesting complex from Ectothiorhodospira haloalkaliphila is negligible. Photosynth Res 133:289–295CrossRefGoogle Scholar
  39. Reed DW, Peters GA (1972) Characterization of the pigments in reaction center preparations from Rhodopseudomonas sphaeroides. J Biol Chem 247:7148–7152Google Scholar
  40. Tandori J, Mate Z, Maroti P, Vass I (1996) Resistance of reaction centers from Rhodobacter sphaeroides against UV-B radiation. Effects on protein structure and electron transport. Photosynth Res 50:171–179CrossRefGoogle Scholar
  41. Tokaji Z, Tandori J, Maroti P (2002) Light- and redox-dependent thermal stability of the reaction center of the photosynthetic bacterium Rhodobacter sphaeroides. Photochem Photobiol 75:605–612CrossRefGoogle Scholar
  42. Uchoa AF, Knox PP, Turchielle R, Seifullina NK, Baptista MS (2008) Singlet oxygen generation in the reaction centers of Rhodobacter sphaeroides. Eur Biophys J 37:843–850CrossRefGoogle Scholar
  43. Vass I, Sass L, Spetea C, Bakou A, Ghanotakis DF, Petrouleas V (1996) UV-B-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Impairment of donor and acceptor side components. Biochemistry 35:8964–8973CrossRefGoogle Scholar
  44. Williams W, Gounaris K (1992) Stabilisation 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
  45. Zacharie U, Lancaster CRD (2001) Proton uptake associated with the reduction of the primary quinone QA influences the binding site of the secondary quinone QB in Rhodopseudomonas viridis photosynthetic reaction centers. Biochim Biophys Acta 1505:280–290CrossRefGoogle Scholar
  46. Zagidullin VE, Lukashev EP, Knox PP, Seifullina NK, Sokolova OS, Pechnikova EV, Lokstein H, Paschenko VZ (2014) Properties of hybrid complexes composed of photosynthetic reaction centers from the purple bacterium Rhodobacter sphaeroides and quantum dots in lecithin liposomes. Biochemistry 79:1183–1191Google Scholar
  47. Zakharova NI, Churbanova IY (2000) Methods for isolating reaction center preparations from purple photosynthetic bacteria. Biochemistry 65:181–193Google Scholar
  48. Zhang G, Zhu B, Nakamura Y, Shimoishi Y, Murata Y (2008) Structure-dependent photodegradation of carotenoids accelerated by dimethyl tetrasulfide under UVA irradiation. Biosci Biotechnol Biochem 72:2176–2183CrossRefGoogle Scholar
  49. Zhang N, Liu F-F, Dong X-Y, Sun Y (2012) Molecular insight into the counteraction of trehalose on urea-induced protein denaturation using molecular dynamics simulation. J Phys Chem B 116:7040–7047CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Peter P. Knox
    • 1
  • Evgeny P. Lukashev
    • 1
  • Vladimir V. Gorokhov
    • 1
  • Nadezhda P. Grishanova
    • 1
  • Vladimir Z. Paschenko
    • 1
    Email author
  1. 1.Department of BiophysicsBiological Faculty of the M.V. Lomonosov Moscow State UniversityMoscowRussia

Personalised recommendations