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Photosynthesis Research

, Volume 136, Issue 3, pp 379–392 | Cite as

Characterization of mercury(II)-induced inhibition of photochemistry in the reaction center of photosynthetic bacteria

  • Gábor Sipka
  • Mariann Kis
  • Péter MarótiEmail author
Original Article

Abstract

Mercuric contamination of aqueous cultures results in impairment of viability of photosynthetic bacteria primarily by inhibition of the photochemistry of the reaction center (RC) protein. Isolated reaction centers (RCs) from Rhodobacter sphaeroides were exposed to Hg2+ ions up to saturation concentration (~ 103 [Hg2+]/[RC]) and the gradual time- and concentration-dependent loss of the photochemical activity was monitored. The vast majority of Hg2+ ions (about 500 [Hg2+]/[RC]) had low affinity for the RC [binding constant Kb ~ 5 mM−1] and only a few (~ 1 [Hg2+]/[RC]) exhibited strong binding (Kb ~ 50 μM−1). Neither type of binding site had specific and harmful effects on the photochemistry of the RC. The primary charge separation was preserved even at saturation mercury(II) concentration, but essential further steps of stabilization and utilization were blocked already in the 5 < [Hg2+]/[RC] < 50 range whose locations were revealed. (1) The proton gate at the cytoplasmic site had the highest affinity for Hg2+ binding (Kb ~ 0.2 μM−1) and blocked the proton uptake. (2) Reduced affinity (Kb ~ 0.05 μM−1) was measured for the mercury(II)-binding site close to the secondary quinone that resulted in inhibition of the interquinone electron transfer. (3) A similar affinity was observed close to the bacteriochlorophyll dimer causing slight energetic changes as evidenced by a ~ 30 nm blue shift of the red absorption band, a 47 meV increase in the redox midpoint potential, and a ~ 20 meV drop in free energy gap of the primary charge pair. The primary quinone was not perturbed upon mercury(II) treatment. Although the Hg2+ ions attack the RC in large number, the exertion of the harmful effect on photochemistry is not through mass action but rather a couple of well-defined targets. Bound to these sites, the Hg2+ ions can destroy H-bond structures, inhibit protein dynamics, block conformational gating mechanisms, and modify electrostatic profiles essential for electron and proton transfer.

Keywords

Bacterial photosynthesis Bacteriochlorophyll absorption spectroscopy Bacteriochlorophyll fluorescence spectroscopy Bioenergetics Mercury(II) contamination Quinones 

Abbreviations

BChl

Bacteriochlorophyll

BPhe

Bacteriopheophytin

cyt c2+

Reduced cytochrome c

DF

Delayed fluorescence

LDAO

Lauryl dimethylamine N-oxide

NEM

N-ethylmaleimide

P

Bacteriochlorophyll dimer

pCMB

p-Chloromercuribenzoate

PF

Prompt fluorescence

QA

Primary acceptor (ubiquinone)

QB

Secondary acceptor

Rba

Rhodobacter

RC

Reaction center

Notes

Acknowledgements

We are grateful to Prof. James Smart (Department of Biological Sciences, University of Tennessee at Martin, USA) for valuable discussions and gratefully acknowledge financial support from GINOP-2.3.2-15-2016-00001, OTKA-K 112688, Photosynthesis—Life from Light—Foundation (Hungary) (GS), COST (CM1306), and EFOP-3.6.2-16-2017-0005 (MK and PM).

References

  1. Allen JP, Williams JC (1995) Relationship between the oxidation potential of the bacteriochlorophyll dimer and electron transfer in photosynthetic reaction centers. J Bioenerg Biomembr 27(3):275–283.  https://doi.org/10.1007/Bf02110097 PubMedCrossRefGoogle Scholar
  2. Andréasson U, Andréasson LE (2003) Characterization of a semi-stable, charge-separated state in reaction centers from Rhodobacter sphaeroides. Photosynth Res 75(3):223–233.  https://doi.org/10.1023/A:1023944605460 PubMedCrossRefGoogle Scholar
  3. Arata H, Parson WW (1981) Delayed fluorescence from Rhodopseudomonas sphaeroides reaction centers—enthalpy and free-energy changes accompanying electron-transfer from P870 to quinones. Biochim Biophys Acta 638(2):201–209.  https://doi.org/10.1016/0005-2728(81)90228-0 CrossRefGoogle Scholar
  4. Asztalos E, Maróti P (2009) Export or recombination of charges in reaction centers in intact cells of photosynthetic bacteria. Biochim Biophys Acta 1787(12):1444–1450.  https://doi.org/10.1016/j.bbabio.2009.06.007 PubMedCrossRefGoogle Scholar
  5. Asztalos E, Italiano F, Milano F, Maróti P, Trotta M (2010) Early detection of mercury contamination by fluorescence induction of photosynthetic bacteria. Photochem Photobiol Sci 9(9):1218–1223.  https://doi.org/10.1039/c0pp00040j PubMedCrossRefGoogle Scholar
  6. Asztalos E, Sipka G, Kis M, Trotta M, Maróti P (2012) The reaction center is the sensitive target of the mercury(II) ion in intact cells of photosynthetic bacteria. Photosynth Res 112(2):129–140.  https://doi.org/10.1007/s11120-012-9749-2 PubMedCrossRefGoogle Scholar
  7. Axelrod HL, Abresch EC, Paddock ML, Okamura MY, Feher G (2000) Determination of the binding sites of the proton transfer inhibitors Cd2+ and Zn2+ in bacterial reaction centers. Proc Natl Acad Sci USA 97(4):1542–1547.  https://doi.org/10.1073/pnas.97.4.1542 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Brzezinski P, Andreasson LE (1995) Trypsin treatment of reaction centers from Rhodobacter sphaeroides in the dark and under illumination: protein structural changes follow charge separation. Biochemistry 34(22):7498–7506.  https://doi.org/10.1021/bi00022a025 PubMedCrossRefGoogle Scholar
  9. Chen L, Zhang J, Zhub Y, Zhang Y (2015) Molecular interaction of inorganic mercury(II) with catalase: a spectroscopic study in combination with molecular docking. RSC Adv 5(97):79874–79881.  https://doi.org/10.1039/C5RA15301H CrossRefGoogle Scholar
  10. Chunmei D, Cunwei J, Huixiang L, Yuze S, Wei Y, Dan Z (2014) Study of the interaction between mercury (II) and bovine serum albumin by spectroscopic methods. Environ Toxicol Phar 37(2):870–877.  https://doi.org/10.1016/j.etap.2014.01.021 CrossRefGoogle Scholar
  11. Debus RJ, Feher G, Okamura MY (1985) LM complex of reaction centers from Rhodopseudomonas sphaeroides R-26—characterization and reconstitution with the H-subunit. Biochemistry 24(10):2488–2500.  https://doi.org/10.1021/bi00331a015 CrossRefGoogle Scholar
  12. Deng C, Zhang D, Pan X, Chang F, Wang S (2013) Toxic effects of mercury on PSI and PSII activities, membrane potential and transthylakoid proton gradient in Microsorium pteropus. J Photochem Photobiol B 127:1–7.  https://doi.org/10.1016/j.jphotobiol.2013.07.012 PubMedCrossRefGoogle Scholar
  13. Deshmukh SS (2013) Molecular assignment of light-induced structural changes using site-directed mutant reaction centers. Concordia University, MontrealGoogle Scholar
  14. Deshmukh SS, Williams JC, Allen JP, Kálmán L (2011) Light-induced conformational changes in photosynthetic reaction centers: redox-regulated proton pathway near the dimer. Biochemistry 50(16):3321–3331.  https://doi.org/10.1021/bi200169y PubMedCrossRefGoogle Scholar
  15. Filus Z, Laczkó G, Wraight CA, Maróti P (2004) Delayed fluorescence from the photosynthetic reaction center measured by electronic gating of the photomultiplier. Biopolymers 74(1–2):92–95.  https://doi.org/10.1002/bip.20051 PubMedCrossRefGoogle Scholar
  16. Fujii R, Adachi S, Roszak AW, Gardiner AT, Cogdell RJ, Isaacs NW, Koshihara S, Hashimoto H (2009) Structure of the carotenoid bound to the reaction centre from Rhodobacter sphaeroides 2.4.1 revealed by time-resolved X-ray crystallography.  https://doi.org/10.2210/pdb3i4d/pdb
  17. Gao JL, Wraight CA (1990) Sulfhydryl modifying reagents inhibit QA oxidation in reaction centers from Rhodobacter sphaeroides and capsulatus, but not Rhodopseudomonas viridis. Photosynth Res 26(3):171–179  https://doi.org/10.1007/Bf00033130 PubMedGoogle Scholar
  18. Gast P, Hemelrijk PW, VanGorkom 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(3):805–809PubMedCrossRefGoogle Scholar
  19. Gerencsér L, Maróti P (2001) Retardation of proton transfer caused by binding of the transition metal ion to the bacterial reaction center is due to pK a shifts of key protonatable residues. Biochemistry 40(6):1850–1860.  https://doi.org/10.1021/bi0021636 PubMedGoogle Scholar
  20. Gerencsér L, Laczko G, Maróti P (1999) Unbinding of oxidized cytochrome c from photosynthetic reaction center of Rhodobacter sphaeroides is the bottleneck of fast turnover. Biochemistry 38(51):16866–16875.  https://doi.org/10.1021/bi991563u PubMedCrossRefGoogle Scholar
  21. Giotta L, Agostiano A, Italiano F, Milano F, Trotta M (2006) Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides. Chemosphere 62(9):1490–1499.  https://doi.org/10.1016/j.chemosphere.2005.06.014 PubMedCrossRefGoogle Scholar
  22. Graige MS, Paddock ML, Bruce JM, Feher G, Okamura MY (1996) Mechanism of proton-coupled electron transfer for quinone QB reduction in reaction centers of Rb sphaeroides. J Am Chem Soc 118(38):9005–9016.  https://doi.org/10.1021/Ja960056m CrossRefGoogle Scholar
  23. Greenberg AE, Clesceri LS, Eaton AD (1992) Standard methods for the examination of water and wastewater, 18th edn. Amer Public Health Assn, WashingtonGoogle Scholar
  24. Gregoire DS, Poulain AJ (2014) A little bit of light goes a long way: the role of phototrophs on mercury cycling. Metallomics 6(3):396–407.  https://doi.org/10.1039/c3mt00312d PubMedCrossRefGoogle Scholar
  25. Hellinga HW (1996) Metalloprotein design. Curr Opin Biotechnol 7(4):437–441.  https://doi.org/10.1016/S0958-1669(96)80121-2 PubMedCrossRefGoogle Scholar
  26. Ivancich A, Mattioli TA (1998) A comparative study of conserved protein interactions of the primary electron donor in photosynthetic purple bacterial reaction centers. Photosynth Res 55(2–3):207–215.  https://doi.org/10.1023/A:1006033617734 CrossRefGoogle Scholar
  27. Kálmán L, Maróti P (1994) Stabilization of reduced primary quinone by proton uptake in reaction centers of Rhodobacter sphaeroides. Biochemistry 33(31):9237–9244.  https://doi.org/10.1021/bi00197a027 PubMedCrossRefGoogle Scholar
  28. Kálmán L, Williams JC, Allen JP (2011) Energetics for oxidation of a bound manganese cofactor in modified bacterial reaction centers. Biochemistry 50(16):3310–3320.  https://doi.org/10.1021/bi1017478 PubMedCrossRefGoogle Scholar
  29. Katona G, Snijder A, Gourdon P, Andreasson U, Hansson O, Andreasson LE, Neutze R (2005) Conformational regulation of charge recombination reactions in a photosynthetic bacterial reaction center. Nat Struct Mol Biol 12(7):630–631.  https://doi.org/10.1038/nsmb948 PubMedCrossRefGoogle Scholar
  30. Kis M, Sipka G, Asztalos E, Rázga Z, Maróti P (2015) Purple non-sulfur photosynthetic bacteria monitor environmental stresses. J Photochem Photobiol B 151:110–117.  https://doi.org/10.1016/j.jphotobiol.2015.07.017 PubMedCrossRefGoogle Scholar
  31. Kis M, Sipka G, Maróti P (2017) Stoichiometry and kinetics of mercury uptake by photosynthetic bacteria. Photosynth Res 132(2):197–209.  https://doi.org/10.1007/s11120-017-0357-z PubMedCrossRefGoogle Scholar
  32. Koepke J, Krammer EM, Klingen AR, Sebban P, Ullmann GM, Fritzsch G (2007) pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states. J Mol Biol 371(2):396–409.  https://doi.org/10.1016/j.jmb.2007.04.082 PubMedCrossRefGoogle Scholar
  33. Kriegl JM, Forster FK, Nienhaus GU (2003) Charge recombination and protein dynamics in bacterial photosynthetic reaction centers entrapped in a sol-gel matrix. Biophys J 85(3):1851–1870.  https://doi.org/10.1016/S0006-3495(03)74613-X PubMedPubMedCentralCrossRefGoogle Scholar
  34. Malferrari M, Turina P, Francia F, Mezzetti A, Leibl W, Venturoli G (2015) Dehydration affects the electronic structure of the primary electron donor in bacterial photosynthetic reaction centers: evidence from visible-NIR and light-induced difference FTIR spectroscopy. Photochem Photobiol Sci 14(2):238–251.  https://doi.org/10.1039/c4pp00245h PubMedCrossRefGoogle Scholar
  35. Mäntele W (1993) Reaction-induced infrared difference spectroscopy for the study of protein function and reaction-mechanisms. Trends Biochem Sci 18(6):197–202.  https://doi.org/10.1016/0968-0004(93)90186-Q PubMedCrossRefGoogle Scholar
  36. Maróti P, Govindjee (2016) The two last overviews by Colin Allen Wraight (1945–2014) on energy conversion in photosynthetic bacteria. Photosynth Res 127(2):257–271.  https://doi.org/10.1007/s11120-015-0175-0 PubMedCrossRefGoogle Scholar
  37. Maróti P, Wraight CA (1988) Flash-induced H+ binding by bacterial photosynthetic reaction centers—comparison of spectrophotometric and conductimetric methods. Biochim Biophys Acta 934(3):314–328.  https://doi.org/10.1016/0005-2728(88)90091-6 CrossRefGoogle Scholar
  38. Maróti P, Wraight CA (2008) The redox midpoint potential of the primary quinone of reaction centers in chromatophores of Rhodobacter sphaeroides is pH independent. Eur Biophys J 37(7):1207–1217.  https://doi.org/10.1007/s00249-008-0301-4 PubMedCrossRefGoogle Scholar
  39. McMahon BH, Muller JD, Wraight CA, Nienhaus GU (1998) Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys J 74(5):2567–2587.  https://doi.org/10.1016/S0006-3495(98)77964-0 PubMedPubMedCentralCrossRefGoogle Scholar
  40. McPherson PH, Nagarajan V, Parson WW, Okamura MY, Feher G (1990) pH dependence of the free energy gap between DQA and D+QA determined from delayed fluorescence in reaction centers from Rhodobacter sphaeroides R-26. Biochim Biophys Acta 1019(1):91–94.  https://doi.org/10.1016/0005-2728(90)90128-Q Google Scholar
  41. McPherson PH, Okamura MY, Feher G (1993) Light-induced proton uptake by photosynthetic reaction centers from Rhodobacter sphaeroides R-26.1. II. Protonation of the state DQAQB 2–. Biochim Biophys Acta 1144(3):309–324.  https://doi.org/10.1016/0005-2728(93)90116-W PubMedGoogle Scholar
  42. Milano F, Giotta L, Guascito MR, Agostiano A, Sblendorio S, Valli L, Perna FM, Cicco L, Trotta M, Capriati V (2017) Functional enzymes in nonaqueous environment: the case of photosynthetic reaction centers in deep eutectic solvents. ACS Sustain Chem Eng 5(9):7768–7776.  https://doi.org/10.1021/acssuschemeng.7b01270 CrossRefGoogle Scholar
  43. Müh F, Rautter J, Lubitz W (1997) Two distinct conformations of the primary electron donor in reaction centers from Rhodobacter sphaeroides revealed by ENDOR/TRIPLE-spectroscopy. Biochemistry 36(14):4155–4162.  https://doi.org/10.1021/bi962859s PubMedCrossRefGoogle Scholar
  44. Müh F, Schulz C, Schlodder E, Jones MR, Rautter J, Kuhn M, Lubitz W (1998) Effects of zwitterionic detergents on the electronic structure of the primary donor and the charge recombination kinetics of P+QA in native and mutant reaction centers from Rhodobacter sphaeroides. Photosynth Res 55(2–3):199–205.  https://doi.org/10.1023/A:1005960003482 Google Scholar
  45. Okamura MY, Isaacson RA, Feher G (1975) Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc Natl Acad Sci USA 72(9):3491–3495.  https://doi.org/10.1073/pnas.72.9.3491 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458(1):148–163.  https://doi.org/10.1016/S0005-2728(00)00065-7 PubMedCrossRefGoogle Scholar
  47. Paddock ML, Graige MS, Feher G, Okamura MY (1999) Identification of the proton pathway in bacterial reaction centers: inhibition of proton transfer by binding of Zn2+ or Cd2+. Proc Natl Acad Sci USA 96(11):6183–6188.  https://doi.org/10.1073/pnas.96.11.6183 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Paddock ML, Flores M, Isaacson R, Chang C, Abresch EC, Okamura MY (2007) ENDOR spectroscopy reveals light induced movement of the H-bond from Ser-L223 upon forming the semiquinone (QB –*) in reaction centers from Rhodobacter sphaeroides. Biochemistry 46(28):8234–8243.  https://doi.org/10.1021/bi7005256 PubMedPubMedCentralGoogle Scholar
  49. Rinyu L, Martin EW, Takahashi E, Maróti P, Wraight CA (2004) Modulation of the free energy of the primary quinone acceptor (QA) in reaction centers from Rhodobacter sphaeroides: contributions from the protein and protein-lipid(cardiolipin) interactions. BBA-Bioenergetics 1655(1–3):93–101.  https://doi.org/10.1016/j.bbabio.2003.07.012 PubMedCrossRefGoogle Scholar
  50. Shlyk O, Samish I, Matenova M, Dulebo A, Polakova H, Kaftan D, Scherz A (2017) A single residue controls electron transfer gating in photosynthetic reaction centers. Sci Rep-Uk 7.  https://doi.org/10.1038/Srep44580
  51. Stowell MH, McPhillips TM, Rees DC, Soltis SM, Abresch E, Feher G (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science 276(5313):812–816.  https://doi.org/10.1126/science.276.5313.812 PubMedCrossRefGoogle Scholar
  52. Theraulaz F, Thomas OP (1994) Complexometric determination of mercury(II) in waters by spectrophotometry of its dithizone complex. Mikrochim Acta 113(1–2):53–59.  https://doi.org/10.1007/BF01243137 CrossRefGoogle Scholar
  53. Thielges M, Uyeda G, Camara-Artigas A, Kálmán L, Williams JC, Allen JP (2005) Design of a redox-linked active metal site: Manganese bound to bacterial reaction centers at a site resembling that of photosystem II. Biochemistry 44(20):7389–7394.  https://doi.org/10.1021/bi050377n PubMedCrossRefGoogle Scholar
  54. Timpmann K, Kangur L, Lohmus A, Freiberg A (2017) High-pressure modulation of the structure of the bacterial photochemical reaction center at physiological and cryogenic temperatures. J Phys B 50 (14).  https://doi.org/10.1088/1361-6455/Aa77e4
  55. Turzó K, Laczkó G, Filus Z, Maróti P (2000) Quinone-dependent delayed fluorescence from the reaction center of photosynthetic bacteria. Biophys J 79(1):14–25.  https://doi.org/10.1016/S0006-3495(00)76270-9 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Utschig LM, Thurnauer NC (2004) Metal ion modulated electron transfer in photosynthetic proteins. Acc Chem Res 37(7):439–447.  https://doi.org/10.1021/ar020197v PubMedCrossRefGoogle Scholar
  57. Utschig LM, Ohigashi Y, Thurnauer MC, Tiede DM (1998) A new metal-binding site in photosynthetic bacterial reaction centers that modulates QA to QB electron transfer. Biochemistry 37(23):8278–8281.  https://doi.org/10.1021/Bi980395n PubMedCrossRefGoogle Scholar
  58. Utschig LM, Thurnauner MC, Tiede DM, Poluektov OG (2005) Low-temperature interquinone electron transfer in photosynthetic reaction centers from Rhodobacter sphaeroides and Blastochloris viridis: characterization of QB states by high-frequency electron paramagnetic resonance (EPR) and electron-nuclear double resonance (ENDOR). Biochemistry 44(43):14131–14142.  https://doi.org/10.1021/bi051060q PubMedGoogle Scholar
  59. van Mourik F, Reus M, Holzwarth AR (2001) Long-lived charge-separated states in bacterial reaction centers isolated from Rhodobacter sphaeroides. BBA-Bioenergetics 1504(2–3):311–318.  https://doi.org/10.1016/S0005-2728(00)00259-0 PubMedCrossRefGoogle Scholar
  60. Vasilieva LG, Fufina TY, Gabdulkhakov AG, Leonova MM, Khatypov RA, Shuvalov VA (2012) The site-directed mutation I(L177)H in Rhodobacter sphaeroides reaction center affects coordination of PA and BB bacteriochlorophylls. Biochim Biophys Acta 1817(8):1407–1417.  https://doi.org/10.1016/j.bbabio.2012.02.008 PubMedCrossRefGoogle Scholar
  61. Wang S, Lin S, Lin X, Woodbury NW, Allen JP (1994) Comparative study of reaction centers from purple photosynthetic bacteria: isolation and optical spectroscopy. Photosynth Res 42(3):203–215.  https://doi.org/10.1007/BF00018263 PubMedCrossRefGoogle Scholar
  62. Woodbury NW, Becker M, Middendorf D, Parson WW (1985) Picosecond kinetics of the initial photochemical electron-transfer reaction in bacterial photosynthetic reaction centers. Biochemistry 24(26):7516–7521.  https://doi.org/10.1021/Bi00347a002 PubMedCrossRefGoogle Scholar
  63. Wraight CA (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front Biosci 9:309–337.  https://doi.org/10.2741/1236 PubMedCrossRefGoogle Scholar
  64. Wraight CA, Clayton RK (1974) The absolute quantum efficiency of bacteriochlorophyll photooxidation in reaction centres of Rhodopseudomonas spheroides. Biochim Biophys Acta 333(2):246–260.  https://doi.org/10.1016/0005-2728(74)90009-7 PubMedCrossRefGoogle Scholar
  65. Wraight CA, Gunner MR (2009) The acceptor quinones of purple photosynthetic bacteria—structure and spectroscopy. In: Hunter CN, Daldal F, Thurnauer M, Beatty JT (eds) The purple phototrophic bacteria. Advances in photosynthesis and respiration, vol 28. Springer, Dordrecht, pp 379–405CrossRefGoogle Scholar
  66. Yruela I, Alfonso M, Dezarate IO, Montoya G, Picorel R (1993) Precise location of the Cu(II)-inhibitory binding site in higher plant and bacterial photosynthetic reaction centers as probed by light-induced absorption changes. J Biol Chem 268(3):1684–1689PubMedGoogle Scholar
  67. Zabelin AA, Fufina TY, Vasilieva LG, Shkuropatova VA, Zvereva MG, Shkuropatov AY, Shuvalov VA (2009) Mutant reaction centers of Rhodobacter sphaeroides I(L177)H with strongly bound bacteriochlorophyll a: structural properties and pigment-protein interactions. Biochemistry (Moscow) 74(1):68–74.  https://doi.org/10.1134/S0006297909010106 CrossRefGoogle Scholar
  68. Zankel KL, Reed DW, Clayton RK (1968) Fluorescence and photochemical quenching in photosynthetic reaction centers. Proc Natl Acad Sci USA 61(4):1243–1249PubMedPubMedCentralCrossRefGoogle Scholar
  69. Zastrow ML, Pecoraro VL (2013) Designing functional metalloproteins: from structural to catalytic metal sites. Coordin Chem Rev 257(17–18):2565–2588.  https://doi.org/10.1016/j.ccr.2013.02.007 CrossRefGoogle Scholar
  70. Zhao HB, Song WY, Han GD, Shao HB, Zhang SW (2014) Dynamic change of wheat eco-physiology and implications for establishing high-efficient stable agro-ecosystems under Hg stress. Ecol Eng 70:50–55.  https://doi.org/10.1016/j.ecoleng.2014.04.022 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Medical PhysicsUniversity of SzegedSzegedHungary
  2. 2.Department of Plant BiologyHungarian Academy of Science, Biological Research CentreSzegedHungary

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