Abstract
The effect of cadmium on the photosynthetic activity of Synechocystis PCC 6803 was monitored in this study. The oxygen evolving capacity of Synechocystis treated with 40 μM CdCl2 was depressed to 10% of the maximum in 15 min, indicating that Cd2+ penetrated rapidly into the cells and blocked the photosynthetic activity. However, neither photosystem II (PSII) nor photosystem I (PSI) activity showed a significant short-term decrease which would explain this fast decrease in the whole-chain electron transport. Thermoluminescence measurements have shown that the charge separation and stabilization in PSII remains essentially unchanged during the first few hours following the Cd2+ treatment. The electron flow through PSI was monitored by following the redox changes of the P700 reaction centers of PSI. Alterations in the oxidation kinetics of P700 in the Cd2+-treated cells indicated that Cd2+ treatment might affect the available electron acceptor pool of P700, including the CO2 reduction and accumulation in the cells. Perturbed angular correlation of γ-rays (PAC) using the radioactive 111mCd isotope was used to follow the Cd2+ uptake at a molecular level. The most plausible interpretation of the PAC data is that Cd2+ is taken up by one or more Zn proteins replacing Zn2+ in Synechocystis PCC 6803. Using the radioactive 109Cd isotope, a protein of approximately 30 kDa that binds Cd2+ could be observed in sodium dodecyl sulfate polyacrylamide gel electrophoresis. The results indicate that Cd2+ might inactivate different metal-containing enzymes, including carbonic anhydrase, by replacing the zinc ion, which would explain the rapid and almost full inhibition of the photosynthetic activity in cyanobacteria.
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Abbreviations
- BASIL:
-
Bauers axially symmetric independent ligands
- CA:
-
Carbonic anhydrase
- CCM:
-
Carbon-concentrating mechanism
- EFG:
-
Electric field gradient
- HEPES:
-
N-(2-Hydroxyethyl)piperazine)-N′-ethanesulfonic acid
- NQI:
-
Nuclear quadrupole interaction
- PAC:
-
Perturbed angular correlation of γ-rays
- PAGE:
-
Polyacrylamide gel electrophoresis
- PQ:
-
Plastoquinone
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- QB :
-
Reduced secondary quinine acceptor
- Rubisco:
-
Ribulose bisphosphate carboxylase-oxygenase
- SDS:
-
Sodium dodecyl sulfate
- Tris:
-
Tris(hydroxymethyl)aminomethane
References
Das P, Samantaray S, Rout GR (1997) Environ Pollut 98:29–36
Prasad MNV (1995) Environ Exp Bot 35:525–545
Seregin IV, Ivanov VB (2001) Russ J Plant Physiol 48:523–544
Ali G, Srivastava PS, Iqbal M (1998) Biol Plant 41:635–639
Ali G, Srivastava PS, Iqbal M (2000) Biol Plant 43:599–601
Carrier P, Baryla A, Havaux M (2003) Planta 216:939–950
Di Cagno R, Guidi L, Stefani A, Soldatini GF (1999) New Phytol 144:65–71
Ghorbanli M, Kaveh SH, Sepehr MF (1999) Photosynthetica 37:627–631
Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas M, del Rio LA (2001) J Exp Bot 52:2115–2126
Vassilev A, Lidon FC, Matos MD, Ramalho JC, Yordanov I (2002) J Plant Nutr 25:2343–2360
Atri N, Rai LC (2003) J Microbiol Biotechnol 13:544–551
Cheng SP, Ren F, Grosse W, Wu ZB (2002) Int J Phytoremediat 4:239–246
Gorbunov MY, Gorbunova EA (1993) Russ J Plant Physiol 40:656–659
Prasad MNV, Malec P, Waloszek A, Bojko M, Strzalka K (2001) Plant Sci 161:881–889
Siedlecka A, Baszynski T (1993) Physiol Plant 87:199–202
Tumova E, Sofrova D (2002) Photosynthetica 40:103–108
Vassilev A, Lidon F, Scotti P, Da Graca M, Yordanov I (2004) Biol Plant 48:153–156
Plekhanov SE, Chemeris YK (2003) Biol Bull 30:506–511
Greger M, Ogren E (1991) Physiol Plant 83:129–135
Krupa Z (1999) Z Naturforsch C 54:723–729
Siedlecka A, Krupa Z (1999) Photosynthetica 36:321–331
Bender J, Lee RF, Phillips P (1995) J Ind Microbiol 14:113–118
El Enany EA, Issa AA (2000) Environ Toxicol Pharmacol 8:95–101
Inthorn D, Nagase H, Isaji Y, Hirata K, Miyamoto K (1996) J Ferment Bioeng 82:580–584
Mohamed ZA (2001) Water Res 35:4405–4409
Prakasham RS, Ramakrishna SV (1998) J Sci Ind Res 57:258–265
Campanella L, Cubadda F, Sammartino MP, Saoncella A (2001) Water Res 35:69–76
Tonnina D, Campanella L, Sammartino MP, Visco G (2002) Ann Chim 92:477–484
Allen MM (1968) J Phycol 4:1
Demeter S, Vass I, Horvath G, Laufer A (1984) Biochim Biophys Acta 764:33–39
Frauenfelder H, Steffen RM (1965) In: Siegbahn K (ed) α- β and γ-ray spectroscopy. North-Holland, Amsterdam, pp 997–1198
Hemmingsen L, Sas KN, Danielsen E (2004) Chem Rev 104:4027–4061
Butz T (1989) Hyperfine Interact 52:189–228
Butz T (1992) Correct Hyperfine Interact 73:387–388
Danielsen E, Bauer R (1990) Hyperfine Interact 62:311–324
Perrin F (1934) J Phys Radium 5:497–511
Butz T, Saibene S, Fraenzke T, Weber M (1989) Nucl Instrum Methods Phys Res A 284:417–421
Bauer R, Jensen SJ, Schmidt-Nielsen B (1988) Hyperfine Interact 39:203–234
Demeter S, Vass I (1984) Biochim Biophys Acta 764:24–32
Rutherford AW, Crofts AR, Inoue Y (1982) Biochim Biophys Acta 682:457–465
Maxwell PC, Biggins J (1977) Biochim Biophys Acta 459:442–450
Yu L, Zhao JD, Muhlenhoff U, Bryant DA, Golbeck JH (1993) Plant Physiol 103:171–180
Bonomi F, Iametti S, Kurtz DM, Ragg EM, Richie KA (1998) J Biol Inorg Chem 3:595–605
Hartwig A (2001) Antioxid Redox Signal 3:625–634
Hartwig A, Asmuss M, Blessing H, Hoffmann S, Jahnke G, Khandelwal S, Pelzer A, Burkle A (2002) Food Chem Toxicol 40:1179–1184
Bonomi F, Ganadu ML, Lubinu G, Pagani S (1994) Eur J Biochem 222:639–644
Bauer R, Limkilde P, Johansen JT (1976) Biochemistry 15:334–341
Bauer R, Christensen C, Johansen JT, Bethune JL, Vallee BL (1979) Biochem Biophys Res Commun 90:679–685
Bauer R (1985) Q Rev Biophys 18:1–64
Hemmingsen L, Bauer R, Bjerrum MJ, Zeppezauer M, Adolph HW, Formicka G, Cedergren-Zeppezauer E (1995) Biochemistry 34:7145–7153
Rensing C, Ghosh M, Rosen BP (1999) J Bacteriol 181:5891–5897
Kopera E, Schwerdtle T, Hartwig A, Bal A (2004) Chem Res Toxicol 17:1452–1458
Raven JA, Evans MCW, Korb RE (1999) Photosynth Res 60:111–149
Lindskog S (1997) Pharmacol Ther 74:1–20
Moroney JV, Bartlett SG, Samuelsson G (2001) Plant Cell Environ 24:141–153
Smith KS, Ferry JG (2000) FEMS Microbiol Rev 24:335–366
So AKC, Espie GS (2005) Can J Bot 83:721–734
Kaplan A, Reinhold L (1999) Annu Rev Plant Physiol Plant Mol Biol 50:539–570
Badger MR (2003) Photosynth Res 77:83–94
Badger MR, Price GD (2003) J Exp Bot 54:609–622
Hanson DT, Franklin LA, Samuelsson G, Badger MR (2003) Plant Physiol 132:2267–2275
Smith EC, Griffiths H (2000) New Phytol 145:29–37
Thoms S, Pahlow M, Wolf-Gladrow DA (2001) J Theor Biol 208:295–313
Moskvin OV, Shutova TV, Khristin MS, Ignatova KL, Villarejo A, Samuelsson G, Klimov VV, Ivanov BN (2004) Photosynth Res 79:93–100
Stemler AJ (1997) Physiol Plant 99:348–353
van Hunnik E, Sultemeyer D (2002) Funct Plant Biol 29:243–249
Villarejo A, Shutova T, Moskvin O, Forssen M, Klimov VV, Samuelsson G (2002) EMBO J 21:1930–1938
So AKC, John-McKay M, Espie GS (2002) Planta 214:456–467
Aravind P, Prasad MNV (2004) J Anal Atom Spectrom 19:52–57
Pawlik B, Skowronski T, Ramazanow Z, Gardestrom P, Samuelsson G (1993) Environ Exp Bot 33:331–337
Lindskog S, Malmstrom BG (1962) J Biol Chem 237:1129–1137
Lionetto MG, Caricato R, Erroi E, Giordano ME, Schettino T (2005) Int J Environ Anal Chem 85:895–903
Wang B, Liu CQ, Wu Y (2005) Bull Environ Contam Toxicol 74:227–233
Vitale AM, Monserrat JM, Castilho P, Rodriguez EM (1999) Comp Biochem Phys C 122:121–129
Iverson TM, Alber BE, Kisker C, Ferry JG, Rees DC (2000) Biochemistry 39:9222–9231
Mitsuhashi S, Mizushima T, Yamashita E, Yamamoto M, Kumasaka T, Moriyama H, Ueki T, Miyachi S, Tsukihara T (2000) J Biol Chem 275:5521–5526
Bauer R (1976) PhD thesis
Bauer R, Limkilde P, Johansen JT (1977) Carlberg Res Commun 42:325–339
Acknowledgements
We thank Marianne Lund Jensen for technical assistance. We thank also Anna Haldrup and Poul Erik Jensen for their help with biochemical facilities. This project was supported by the Danish Technical Research Council (9901473), the EU Research Training Network “Transient” (HPRN-CT-1999-00095) and the Hungarian Science Foundation OTKA (T 034188).
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Sas, K.N., Kovács, L., Zsίros, O. et al. Fast cadmium inhibition of photosynthesis in cyanobacteria in vivo and in vitro studies using perturbed angular correlation of γ-rays. J Biol Inorg Chem 11, 725–734 (2006). https://doi.org/10.1007/s00775-006-0113-x
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DOI: https://doi.org/10.1007/s00775-006-0113-x