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Molecular rearrangements of thylakoids after heavy metal poisoning, as seen by Fourier transform infrared (FTIR) and electron spin resonance (ESR) spectroscopy

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Abstract

The specific effects exerted by different heavy metals on both the function and the structure of the photosynthetic apparatus were addressed. The functional analysis performed via the fluorescence induction kinetics revealed that the applied toxic heavy metals can be classified into two groups: Cd and Ni had no significant effect on the photosynthetic electron transport, while Cu, Pb and Zn strongly inhibited the Photosystem II (PS II) activity, as evidenced by the dramatic decreases in both the variable (Fv) and the maximal (Fm) fluorescence. The structural effects of the heavy metal ions on the thylakoid membranes were considered in three relations: (1) lipids, (2) proteins — studied by Fourier transform infrared (FTIR) spectroscopy, and (3) lipid—protein interactions — investigated by electron spin resonance (ESR) spectroscopy using spin-labeled probe molecules. The studied heavy metal ions had only a non-specific rigidifying effect on the thylakoid lipids. As regards proteins, Cd and Ni had no effect on the course of their heat denaturation. The heat denaturation of the proteins was accompanied by a decrease in the α-helix content (1656 cm-1), a parallel increase in the disordered segments (1651 cm-1), a decrease in the intramolecular β-sheet (1636 cm-1) content and the concomitant appearance of an intermolecular β-structure (1621 cm-1). In contrast with Cd and Ni, Cu and Zn blocked the appearance of the intermolecular β-structure. Pb represented an intermediate case. It seems that these heavy metals alter the native membrane structure in such a way that heat-induced aggregation becomes more limited. The ESR data revealed that certain heavy metals also affect the lipid—protein interactions. While Cd and Ni had hardly any effect on the solvation fraction of thylakoid lipids, Cu, Pb and Zn increased the fraction of lipids solvating the proteins. On the basis of the FTIR and ESR data, it seems that Cu, Pb, and Zn increase the surfaces available for lipid—protein interactions by dissociating membrane protein complexes, and that these ‘lipidated’ proteins have a smaller chance to aggregate upon heat denaturation. The data presented here indicate that the damaging effects of poisonous heavy metals are element-specific, Cu, Pb and Zn interact directly with the thylakoid membranes of the photosynthetic apparatus, while Cd and Ni interfere rather with other metabolic processes of plants.

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References

  • Arellano JB, Sröder WP, Sandman G, Chueca A and Barón M (1994) Removal of nuclear contaminants and of non-specifically Photosytem II-bound copper from Photosystem II preparations. Physiol Plant 91: 369–374

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • Arrondo JLR, Muga A, Castresana J and Goñi FM (1993) Quantitative studies of the structure of proteins in solution by Fourier transform infrared spectroscopy. Prog Biophys Mol Biol 59: 23–56

    PubMed  Google Scholar 

  • Barón M, Arellano JB and López-Gorgé J (1995) Copper and Photosystem II: A controversal relationship. Physiol Plant 94: 174–180

    Google Scholar 

  • Baszynski T (1986) Heavy metals as factors affecting photosynthetic apparatus activity. Folia Physiol Cytol Gen 1: 7–27

    Google Scholar 

  • Bellamy LJ (1975) The Infra-Red Spectra of Complex Molecules. Chapman Hall, London.

    Google Scholar 

  • Berliner LJ (1976, 1979) Spin Labeling: Theory and Applications, Vol 1 and Vol 2, Academic Press, New York

    Google Scholar 

  • Berthold DA, Babcock GT and Yocum CA (1986) A highly resolved, oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–234

    Google Scholar 

  • Casal HL and Mantsch HH (1984) Polymorphic phase behaviour of phospholipid membranes studied by infrared spectroscopy. Biochim Biophys Acta 779: 381–401

    PubMed  Google Scholar 

  • Clijsters H and Van Assche F (1985) Inhibition of photosynthesis by heavy metals. Photosynth Res 7: 31–40

    Google Scholar 

  • De Las Rivas J and Barber J (1997) Structure and thermal stability of Photosystem II reaction centers studied by infrared spectroscopy. Biochemistry 36: 8897–8903

    PubMed  Google Scholar 

  • Droppa M and Horváth G (1990) The role of copper in photosynthesis. Crit Rev Plant Sci 9: 111–123

    Google Scholar 

  • Droppa M, Masojidek J, Rózsa Zs, Wolak A, Horváth LI, Farkas T and Horváth G (1987) Characteristics of Cu deficiency-induced inhibition of photosynthetic electron transport in spinach chloroplasts. Biochim Biophys Acta 891: 75–84

    Google Scholar 

  • Gallego SM, Benavides MP and Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: Evidence for involvement of oxidative stress. Plant Sci 121: 151–159

    Google Scholar 

  • Gounaris K, Brain ARR, Quinn PJ and Williams WP (1984) Structural reorganisation of chloroplast thylakoid membranes in response to heat-stress. Biochim Biophys Acta 766: 198–208

    Google Scholar 

  • Horváth G, Droppa M, Fodorpataki L, Istókovics A, Garab Gy and Oettmeier W (1996) Acridones: A chemically new group of protonophores. Proc Natl Acad Sci USA 93: 3876–3880

    PubMed  Google Scholar 

  • Horváth LI (1994) Spin label EPR study of molecular dynamics at lipid/protein association in membranes. In: Hilderson HJ and Ralston GB (eds) Subcellular Biochemistry. Physicochemical Methods in the Study of Biomembranes, Vol 23, pp 205–245. Plenum Press, New York

    Google Scholar 

  • Horváth LI, Brophy PJ and Marsh D (1988) Exchange rates at the lipid – protein interface of myelin proteolipid protein studied by spin label electron spin resonance. Biochemistry 27: 46–52

    PubMed  Google Scholar 

  • Invancich A, Horváth LI, Droppa M, Horváth G and Farkas T (1994) Spin label ESR study of lipid solvation of supramolecular photosynthetic protein complexes in thylakoids. Biochim Biophys Acta 1196: 51–56

    PubMed  Google Scholar 

  • Jackson M, Haris PI and Chapman D (1991) Fourier transform infrared spectroscopic studies of Ca++-binding proteins. Biochemistry 30: 9681–9686

    PubMed  Google Scholar 

  • Jordan BR, Chow WS and Baker A (1983) The role of phospholipids in the molecular organisation of pea chloroplast membranes. Biochim Biophys Acta 725: 77–83

    Google Scholar 

  • Krupa Z and Baszynski T (1995) Some aspects of heavy metal toxicity towards photosynthetic apparatus – direct and indirect effects on light and dark reactions. Acta Physiol Plant 17: 177–190

    Google Scholar 

  • Malik D, Sheoran IS and Singh R (1992) Carbon metabolism in leaves of cadmium treated wheat seedlings. Plant Physiol Biochem 30: 223–229

    Google Scholar 

  • Mantsch HH and McElhaney RN (1991) Phospholipid phase transitions in model and biological membranes as studied by infrared spectroscopy. Chem Phys Lipids 57: 213–226

    PubMed  Google Scholar 

  • Mantsch HH, Martin A and Cameron DG (1981) Characterisation by infrared spectroscopy of the bilayer to nonbilayer phase transition of phosphatidylethanolamines. Biochemistry 20: 3138–3145

    PubMed  Google Scholar 

  • Meharg AA (1994) Integrated tolerance mechanisms: constitutive and adaptive plant responses to elevated metal concentrations in the environment. Plant Cell Environ 17: 989–993

    Google Scholar 

  • Mendelsohn R and Senak L (1993) Quantitative determination of conformational disorder in biological membranes by FTIR spectroscopy. In: Clark RJH and Hester RE (eds) Biomolecular Spectroscopy, Part A, pp 339–380. John Wiley & Sons, Chichester

    Google Scholar 

  • Moore DJ and Mendelsohn R (1994) Adaptation to altered growth temperatures in Acholeplasma laidlawii B: Fourier transform infrared studies of acyl chain conformational order in live cells. Biochemistry 33: 4080–4085

    PubMed  Google Scholar 

  • Moore DJ Sills RH and Mendelsohn R (1995) Peroxidation of erythrocytes: FTIR spectroscopy studies of extracted lipids, isolated membranes and intact cells. Biospectroscopy 1: 133–142

    Google Scholar 

  • Muga A, Arrondo JLR, Bellon T, Sancho J and Bernabeu C (1993) Structural and functional studies on the interaction of sodium dodecyl sulfate with β-galactosidase. Arch Biochem Biophys 300: 451–457

    PubMed  Google Scholar 

  • Naumann D, Schultz C, Görne-Tselnokow U and Hucho F (1993) Secondary structure and temperature behavior of the acethylcholine receptor by Fourier transform infrared spectroscopy. Biochemistry 32: 3162–3168

    PubMed  Google Scholar 

  • Sandmann G and Böger P (1980) Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiol 66: 797–800

    Google Scholar 

  • Shioi Y, Tamai H and Sasa T (1978) Effect of copper on photosynthetic electron transport systems in spinach chloroplasts. Plant Cell Physiol 19: 203–209

    Google Scholar 

  • Surewicz WK, Mantsch HH and Chapman D (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: A critical assessment. Biochemistry 32: 389–394

    PubMed  Google Scholar 

  • Taneva SG, Caaveiro JMM, Muga A and Goñi FM (1995) A pathway for the thermal destabilisation of bacteriorhodopsin. FEBS Lett 367: 297–300

    PubMed  Google Scholar 

  • Thomas PG, Dominy PJ, Vigh L, Mansourian AR, Quinn PJ and Williams WP (1986) Increased thermal stability of pigment-protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. Biochim Biophys Acta 849: 131–140

    Google Scholar 

  • Tuba Z and Csintalan Zs (1992) The effect of pollution on the physiological processes in plants. In: Kovács M, Podani J, Tuba Z, Turcsányi G, Csintalan Zs and Meenks JLD (eds) Biological Indicators in Environmental Protection, pp 169–191. Ellis Horwood, Chichester

    Google Scholar 

  • Van Assche F and Clijsters H (1990) Effects of heavy metals on enzyme activity in plants. Plant Cell Environ 13: 195–206

    Google Scholar 

  • Van Stokkum IHM, Linsdell H, Hadden JM, Haris PI, Chapman D and Bloemendal M (1995) Temperature-induced changes in protein structures studied by Fourier transform infrared spectroscopy and global analysis. Biochemistry 34: 10508–10518

    PubMed  Google Scholar 

  • Watts A and de Pont JJHHM (1985, 1986) Protein–Lipid Interactions, Vol 1 and Vol 2. Elsevier, Amsterdam

    Google Scholar 

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Authors
  1. Balázs Szalontai
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  2. László I. Horváth
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  3. Mónika Debreczeny
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  4. Magdolna Droppa
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  5. Gábor Horváth
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Szalontai, B., Horváth, L.I., Debreczeny, M. et al. Molecular rearrangements of thylakoids after heavy metal poisoning, as seen by Fourier transform infrared (FTIR) and electron spin resonance (ESR) spectroscopy. Photosynthesis Research 61, 241–252 (1999). https://doi.org/10.1023/A:1006345523919

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