JBIC Journal of Biological Inorganic Chemistry

, Volume 11, Issue 6, pp 725–734 | Cite as

Fast cadmium inhibition of photosynthesis in cyanobacteria in vivo and in vitro studies using perturbed angular correlation of γ-rays

  • Klára Nárcisz Sas
  • László Kovács
  • Ottó Zsίros
  • Zoltán Gombos
  • Győző Garab
  • Lars Hemmingsen
  • Eva Danielsen
Original Paper

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.

Keywords

Cyanobacteria Synechocystis sp. 6803 Cadmium toxicity Photosynthesis Oxygen-evolving activity 

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

  1. 1.
    Das P, Samantaray S, Rout GR (1997) Environ Pollut 98:29–36PubMedCrossRefGoogle Scholar
  2. 2.
    Prasad MNV (1995) Environ Exp Bot 35:525–545CrossRefGoogle Scholar
  3. 3.
    Seregin IV, Ivanov VB (2001) Russ J Plant Physiol 48:523–544CrossRefGoogle Scholar
  4. 4.
    Ali G, Srivastava PS, Iqbal M (1998) Biol Plant 41:635–639CrossRefGoogle Scholar
  5. 5.
    Ali G, Srivastava PS, Iqbal M (2000) Biol Plant 43:599–601CrossRefGoogle Scholar
  6. 6.
    Carrier P, Baryla A, Havaux M (2003) Planta 216:939–950PubMedGoogle Scholar
  7. 7.
    Di Cagno R, Guidi L, Stefani A, Soldatini GF (1999) New Phytol 144:65–71CrossRefGoogle Scholar
  8. 8.
    Ghorbanli M, Kaveh SH, Sepehr MF (1999) Photosynthetica 37:627–631CrossRefGoogle Scholar
  9. 9.
    Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas M, del Rio LA (2001) J Exp Bot 52:2115–2126PubMedGoogle Scholar
  10. 10.
    Vassilev A, Lidon FC, Matos MD, Ramalho JC, Yordanov I (2002) J Plant Nutr 25:2343–2360CrossRefGoogle Scholar
  11. 11.
    Atri N, Rai LC (2003) J Microbiol Biotechnol 13:544–551Google Scholar
  12. 12.
    Cheng SP, Ren F, Grosse W, Wu ZB (2002) Int J Phytoremediat 4:239–246CrossRefGoogle Scholar
  13. 13.
    Gorbunov MY, Gorbunova EA (1993) Russ J Plant Physiol 40:656–659Google Scholar
  14. 14.
    Prasad MNV, Malec P, Waloszek A, Bojko M, Strzalka K (2001) Plant Sci 161:881–889CrossRefGoogle Scholar
  15. 15.
    Siedlecka A, Baszynski T (1993) Physiol Plant 87:199–202CrossRefGoogle Scholar
  16. 16.
    Tumova E, Sofrova D (2002) Photosynthetica 40:103–108CrossRefGoogle Scholar
  17. 17.
    Vassilev A, Lidon F, Scotti P, Da Graca M, Yordanov I (2004) Biol Plant 48:153–156CrossRefGoogle Scholar
  18. 18.
    Plekhanov SE, Chemeris YK (2003) Biol Bull 30:506–511CrossRefGoogle Scholar
  19. 19.
    Greger M, Ogren E (1991) Physiol Plant 83:129–135CrossRefGoogle Scholar
  20. 20.
    Krupa Z (1999) Z Naturforsch C 54:723–729Google Scholar
  21. 21.
    Siedlecka A, Krupa Z (1999) Photosynthetica 36:321–331CrossRefGoogle Scholar
  22. 22.
    Bender J, Lee RF, Phillips P (1995) J Ind Microbiol 14:113–118CrossRefGoogle Scholar
  23. 23.
    El Enany EA, Issa AA (2000) Environ Toxicol Pharmacol 8:95–101PubMedCrossRefGoogle Scholar
  24. 24.
    Inthorn D, Nagase H, Isaji Y, Hirata K, Miyamoto K (1996) J Ferment Bioeng 82:580–584CrossRefGoogle Scholar
  25. 25.
    Mohamed ZA (2001) Water Res 35:4405–4409PubMedCrossRefGoogle Scholar
  26. 26.
    Prakasham RS, Ramakrishna SV (1998) J Sci Ind Res 57:258–265Google Scholar
  27. 27.
    Campanella L, Cubadda F, Sammartino MP, Saoncella A (2001) Water Res 35:69–76PubMedCrossRefGoogle Scholar
  28. 28.
    Tonnina D, Campanella L, Sammartino MP, Visco G (2002) Ann Chim 92:477–484PubMedGoogle Scholar
  29. 29.
    Allen MM (1968) J Phycol 4:1CrossRefGoogle Scholar
  30. 30.
    Demeter S, Vass I, Horvath G, Laufer A (1984) Biochim Biophys Acta 764:33–39CrossRefGoogle Scholar
  31. 31.
    Frauenfelder H, Steffen RM (1965) In: Siegbahn K (ed) α- β and γ-ray spectroscopy. North-Holland, Amsterdam, pp 997–1198Google Scholar
  32. 32.
    Hemmingsen L, Sas KN, Danielsen E (2004) Chem Rev 104:4027–4061PubMedCrossRefGoogle Scholar
  33. 33.
    Butz T (1989) Hyperfine Interact 52:189–228CrossRefGoogle Scholar
  34. 34.
    Butz T (1992) Correct Hyperfine Interact 73:387–388CrossRefGoogle Scholar
  35. 35.
    Danielsen E, Bauer R (1990) Hyperfine Interact 62:311–324CrossRefGoogle Scholar
  36. 36.
    Perrin F (1934) J Phys Radium 5:497–511CrossRefGoogle Scholar
  37. 37.
    Butz T, Saibene S, Fraenzke T, Weber M (1989) Nucl Instrum Methods Phys Res A 284:417–421CrossRefGoogle Scholar
  38. 38.
    Bauer R, Jensen SJ, Schmidt-Nielsen B (1988) Hyperfine Interact 39:203–234CrossRefGoogle Scholar
  39. 39.
    Demeter S, Vass I (1984) Biochim Biophys Acta 764:24–32CrossRefGoogle Scholar
  40. 40.
    Rutherford AW, Crofts AR, Inoue Y (1982) Biochim Biophys Acta 682:457–465CrossRefGoogle Scholar
  41. 41.
    Maxwell PC, Biggins J (1977) Biochim Biophys Acta 459:442–450PubMedCrossRefGoogle Scholar
  42. 42.
    Yu L, Zhao JD, Muhlenhoff U, Bryant DA, Golbeck JH (1993) Plant Physiol 103:171–180PubMedGoogle Scholar
  43. 43.
    Bonomi F, Iametti S, Kurtz DM, Ragg EM, Richie KA (1998) J Biol Inorg Chem 3:595–605CrossRefGoogle Scholar
  44. 44.
    Hartwig A (2001) Antioxid Redox Signal 3:625–634PubMedCrossRefGoogle Scholar
  45. 45.
    Hartwig A, Asmuss M, Blessing H, Hoffmann S, Jahnke G, Khandelwal S, Pelzer A, Burkle A (2002) Food Chem Toxicol 40:1179–1184PubMedCrossRefGoogle Scholar
  46. 46.
    Bonomi F, Ganadu ML, Lubinu G, Pagani S (1994) Eur J Biochem 222:639–644PubMedCrossRefGoogle Scholar
  47. 47.
    Bauer R, Limkilde P, Johansen JT (1976) Biochemistry 15:334–341PubMedCrossRefGoogle Scholar
  48. 48.
    Bauer R, Christensen C, Johansen JT, Bethune JL, Vallee BL (1979) Biochem Biophys Res Commun 90:679–685PubMedCrossRefGoogle Scholar
  49. 49.
    Bauer R (1985) Q Rev Biophys 18:1–64PubMedCrossRefGoogle Scholar
  50. 50.
    Hemmingsen L, Bauer R, Bjerrum MJ, Zeppezauer M, Adolph HW, Formicka G, Cedergren-Zeppezauer E (1995) Biochemistry 34:7145–7153PubMedCrossRefGoogle Scholar
  51. 51.
    Rensing C, Ghosh M, Rosen BP (1999) J Bacteriol 181:5891–5897PubMedGoogle Scholar
  52. 52.
    Kopera E, Schwerdtle T, Hartwig A, Bal A (2004) Chem Res Toxicol 17:1452–1458PubMedCrossRefGoogle Scholar
  53. 53.
    Raven JA, Evans MCW, Korb RE (1999) Photosynth Res 60:111–149CrossRefGoogle Scholar
  54. 54.
    Lindskog S (1997) Pharmacol Ther 74:1–20PubMedCrossRefGoogle Scholar
  55. 55.
    Moroney JV, Bartlett SG, Samuelsson G (2001) Plant Cell Environ 24:141–153CrossRefGoogle Scholar
  56. 56.
    Smith KS, Ferry JG (2000) FEMS Microbiol Rev 24:335–366PubMedCrossRefGoogle Scholar
  57. 57.
    So AKC, Espie GS (2005) Can J Bot 83:721–734CrossRefGoogle Scholar
  58. 58.
    Kaplan A, Reinhold L (1999) Annu Rev Plant Physiol Plant Mol Biol 50:539–570PubMedCrossRefGoogle Scholar
  59. 59.
    Badger MR (2003) Photosynth Res 77:83–94PubMedCrossRefGoogle Scholar
  60. 60.
    Badger MR, Price GD (2003) J Exp Bot 54:609–622PubMedCrossRefGoogle Scholar
  61. 61.
    Hanson DT, Franklin LA, Samuelsson G, Badger MR (2003) Plant Physiol 132:2267–2275PubMedCrossRefGoogle Scholar
  62. 62.
    Smith EC, Griffiths H (2000) New Phytol 145:29–37CrossRefGoogle Scholar
  63. 63.
    Thoms S, Pahlow M, Wolf-Gladrow DA (2001) J Theor Biol 208:295–313PubMedCrossRefGoogle Scholar
  64. 64.
    Moskvin OV, Shutova TV, Khristin MS, Ignatova KL, Villarejo A, Samuelsson G, Klimov VV, Ivanov BN (2004) Photosynth Res 79:93–100PubMedCrossRefGoogle Scholar
  65. 65.
    Stemler AJ (1997) Physiol Plant 99:348–353CrossRefGoogle Scholar
  66. 66.
    van Hunnik E, Sultemeyer D (2002) Funct Plant Biol 29:243–249CrossRefGoogle Scholar
  67. 67.
    Villarejo A, Shutova T, Moskvin O, Forssen M, Klimov VV, Samuelsson G (2002) EMBO J 21:1930–1938PubMedCrossRefGoogle Scholar
  68. 68.
    So AKC, John-McKay M, Espie GS (2002) Planta 214:456–467PubMedCrossRefGoogle Scholar
  69. 69.
    Aravind P, Prasad MNV (2004) J Anal Atom Spectrom 19:52–57CrossRefGoogle Scholar
  70. 70.
    Pawlik B, Skowronski T, Ramazanow Z, Gardestrom P, Samuelsson G (1993) Environ Exp Bot 33:331–337CrossRefGoogle Scholar
  71. 71.
    Lindskog S, Malmstrom BG (1962) J Biol Chem 237:1129–1137PubMedGoogle Scholar
  72. 72.
    Lionetto MG, Caricato R, Erroi E, Giordano ME, Schettino T (2005) Int J Environ Anal Chem 85:895–903CrossRefGoogle Scholar
  73. 73.
    Wang B, Liu CQ, Wu Y (2005) Bull Environ Contam Toxicol 74:227–233PubMedCrossRefGoogle Scholar
  74. 74.
    Vitale AM, Monserrat JM, Castilho P, Rodriguez EM (1999) Comp Biochem Phys C 122:121–129Google Scholar
  75. 75.
    Iverson TM, Alber BE, Kisker C, Ferry JG, Rees DC (2000) Biochemistry 39:9222–9231PubMedCrossRefGoogle Scholar
  76. 76.
    Mitsuhashi S, Mizushima T, Yamashita E, Yamamoto M, Kumasaka T, Moriyama H, Ueki T, Miyachi S, Tsukihara T (2000) J Biol Chem 275:5521–5526PubMedCrossRefGoogle Scholar
  77. 77.
    Bauer R (1976) PhD thesisGoogle Scholar
  78. 78.
    Bauer R, Limkilde P, Johansen JT (1977) Carlberg Res Commun 42:325–339CrossRefGoogle Scholar

Copyright information

© SBIC 2006

Authors and Affiliations

  • Klára Nárcisz Sas
    • 1
  • László Kovács
    • 2
  • Ottó Zsίros
    • 2
  • Zoltán Gombos
    • 2
  • Győző Garab
    • 2
  • Lars Hemmingsen
    • 1
  • Eva Danielsen
    • 3
  1. 1.Department of Natural SciencesRoyal Veterinary and Agricultural UniversityFrederiksberg CDenmark
  2. 2.Institute of Plant Biology, Biological Research CenterHungarian Academy of SciencesSzegedHungary
  3. 3.Nano Science CenterUniversity of CopenhagenCopenhagen ØDenmark

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