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H2O2-Induced Inhibition of Photosynthetic O2 Evolution by Anabaena variabilis Cells

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Abstract

Hydrogen peroxide inhibits photosynthetic O2 evolution. It has been shown that H2O2 destroys the function of the oxygen-evolving complex (OEC) in some chloroplast and Photosystem (PS) II preparations causing release of manganese from the OEC. In other preparations, H2O2 did not cause or caused only insignificant release of manganese. In this work, we tested the effect of H2O2 on the photosynthetic electron transfer and the state of OEC manganese in a native system (intact cells of the cyanobacterium Anabaena variabilis). According to EPR spectroscopy data, H2O2 caused an increase in the level of photooxidation of P700, the reaction centers of PS I, and decreased the rate of their subsequent reduction in the dark by a factor larger than four. Combined effect of H2O2, CN, and EDTA caused more than eight- to ninefold suppression of the dark reduction of P700+. EPR spectroscopy revealed that the content of free (or loosely bound) Mn2+ in washed cyanobacterial cells was ∼20% of the total manganese pool. This content remained unchanged upon the addition of CN and increased to 25-30% after addition of H2O2. The content of the total manganese decreased to 35% after the treatment of the cells with EDTA. The level of the H2O2-induced release of manganese increased after the treatment of the cells with EDTA. Incubation of cells with H2O2 for 2 h had no effect on the absorption spectra of the photosynthetic pigments. More prolonged incubation with H2O2 (20 h) brought about degradation of phycobilins and chlorophylla and lysis of cells. Thus, H2O2 causes extraction of manganese from cyanobacterial cells, inhibits the OEC activity and photosynthetic electron transfer, and leads to the destruction of the photosynthetic apparatus. H2O2 is unable to serve as a physiological electron donor in photosynthesis.

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REFERENCES

  1. Debus, R. J. (1992) Biochim. Biophys. Acta, 1102, 269–352.

    PubMed  Google Scholar 

  2. Ananyev, G. M., Zaltsman, L., Vasko, C., and Dismukes, G. C. (2001) Biochim. Biophys. Acta, 1503, 52–68.

    PubMed  Google Scholar 

  3. Metzner, H. (1983) in Bioelectrochem. Proc. Course, Vol. 1, N. Y., pp. 51–113.

    Google Scholar 

  4. Dismukes, G. C., Klimov, V. V., Baranov, S. V., Kozlov, Yu. N., DasGupta, J., and Tyryshkin, A. (2001) Proc. Natl. Acad. Sci. USA, 98, 2170–2175.

    Article  PubMed  Google Scholar 

  5. Radmer, R., and Ollinger, O. (1980) FEBS Lett., 110, 57–61.

    Article  Google Scholar 

  6. Bonini, M. G., Radi, R., Ferrer-Sueta, G., Ferreira, A. M. D. C., and Augusto, O. (1999) J. Biol. Chem., 274, 10802–10806.

    Article  PubMed  Google Scholar 

  7. Koppenol, W. H. (1994) in Free Radical Damage and Its Control (Rice-Evans, C. A., and Burdon, R. H., eds.) Elsevier Sci., pp. 3–24.

  8. Koppenol, W. H., and Rush, J. D. (1987) J. Phys. Chem., 91, 4429–4430.

    Google Scholar 

  9. Ananyev, G., Wydrzynski, T., Renger, G., and Klimov, V. V. (1992) Biochim. Biophys. Acta, 1100, 303–311.

    Google Scholar 

  10. Klimov, V. V., Ananyev, G., Zastryzhnaya, O., Wydryzynski, T., and Renger, G. (1993) Photosynth. Res., 38, 409–416.

    Google Scholar 

  11. Sheptovitsky, Y. G., and Brudvig, G. W. (1998) Biochemistry, 37, 5052–5059.

    Article  PubMed  Google Scholar 

  12. Kelly, P., and Izawa, S. (1978) Biochim. Biophys. Acta., 502, 198–210.

    PubMed  Google Scholar 

  13. Bader, K. P. (1994) Biochim. Biophys. Acta, 1188, 213–219.

    Google Scholar 

  14. Samuilov, V. D. (1997) Biochemistry (Moscow), 62, 451–454.

    Google Scholar 

  15. Blankenship, R. E., and Hartman, H. (1998) Trends Biochem. Sci., 23, 94–97.

    Article  PubMed  Google Scholar 

  16. Velthuys, B., and Kok, B. (1978) Biochim. Biophys. Acta, 502, 211–221.

    PubMed  Google Scholar 

  17. Mano, J., Takahashi, M., and Asada, K. (1987) Biochemistry, 26, 2495–2501.

    Google Scholar 

  18. Sheptovitsky, Y. G., and Brudvig, G. W. (1996) Biochemistry, 35, 16255–16263.

    Article  PubMed  Google Scholar 

  19. Bradley, R. L., Long, K. M., and Frasch, W. D. (1991) FEBS Lett., 286, 209–213.

    Article  PubMed  Google Scholar 

  20. Samuilov, V. D., Bezryadnov, D. V., Gusev, M. V., Kitashov, A. V., and Fedorenko, T. A. (1999) Biochemistry (Moscow), 64, 47–53.

    Google Scholar 

  21. Samuilov, V. D., Bezryadnov, D. V., Gusev, M. V., Kitashov, A. V., and Fedorenko, T. A. (2001) Biochemistry (Moscow), 66, 640–645.

    Article  Google Scholar 

  22. Wydrzynski, T., Ångstrom, J., and Vänngard, T. (1989) Biochim. Biophys. Acta, 973, 23–28.

    Google Scholar 

  23. Sandusky, P. O., and Yocum, C. F. (1988) Biochim. Biophys. Acta, 936, 149–156.

    Google Scholar 

  24. Frasch, W. D., Mei, R., and Sanders, M. A. (1988) Biochemistry, 27, 3715–3719.

    Google Scholar 

  25. Ghanotakis, D. F., Topper, J. N., and Yocum, C. F. (1984) Biochim. Biophys. Acta, 767, 524–531.

    Google Scholar 

  26. Schröder, W. P., and Åkerlund, H.-E. (1986) Biochim. Biophys. Acta, 848, 359–363.

    Google Scholar 

  27. Ishida, H., Shimizu, S., Makino, A., and Mae, T. (1998) Planta, 204, 305–309.

    Article  PubMed  Google Scholar 

  28. Asada, K., and Badger, M. R. (1984) Plant Cell Physiol., 25, 1169–1179.

    Google Scholar 

  29. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y. (1979) J. Gen. Microbiol., 111, 1–61.

    Google Scholar 

  30. Barsky, E. L., Gusev, M. V., Kondrashin, A. A., and Samuilov, V. D. (1982) Biochim. Biophys. Acta, 680, 304–309.

    Google Scholar 

  31. Dawson, R., Elliott, D., Elliott, W., and Jones, K. (1991) Handbook of Biochemist [Russian translation], Mir, Moscow.

  32. Bielski, B. H. J., and Allen, A. O. (1977) J. Phys. Chem., 81, 1048–1050.

    Google Scholar 

  33. Yocum, C., Yerkes, C. T., Blankenship, R., Sharp, R. R., and Babcock, G. T. (1981) Proc. Natl. Acad. Sci. USA, 78, 7507–7511.

    Google Scholar 

  34. Hirano, M., Satoh, K., and Katoh, S. (1980) Photosynth. Res., 1, 149–162.

    Google Scholar 

  35. Lockau, W. (1981) Arch. Microbiol., 128, 336–340.

    Google Scholar 

  36. Peschek, G. A., and Schmetterer, F. (1982) Biochem. Biophys. Res. Commun., 108, 1188–1195.

    PubMed  Google Scholar 

  37. Aples, I., Stürzl, E., Scherer, S., and Böger, P. (1984) Z. Naturforsch., C 39, 623–625.

    Google Scholar 

  38. Abdourashitova, F. D., Barsky, E. L., Gusev, M. V., and Samuilov, V. D. (1985) Planta, 166, 182–186.

    Google Scholar 

  39. Rubin, P. M., Zetooney, E., and McGowan, R. E. (1977) Plant Physiol., 60, 407–411.

    Google Scholar 

  40. Peschek, G. A. (1980) Arch. Microbiol., 125, 123–131.

    Google Scholar 

  41. Finnegan, P. M., Umbach, A. L., and Wilce, J. A. (2003) FEBS Lett., 555, 425–430.

    Article  PubMed  Google Scholar 

  42. Berry, S., Schneider, D., Vermaas, W. F. J., and Rögner, M. (2002) Biochemistry, 41, 3422–3429.

    Article  PubMed  Google Scholar 

  43. Asada, K. (2000) Philos. Trans. R. Soc. Lond. B Biol. Sci., 355, 1419–1431.

    Article  PubMed  Google Scholar 

  44. Mi, H., Endo, T., Schreiber, U., Ogawa, T., and Asada, K. (1992) Plant Cell Physiol., 33, 1233–1237.

    Google Scholar 

  45. Mi, H., Endo, T., Ogawa, T., and Asada, K. (1995) Plant Cell Physiol., 36, 661–668.

    Google Scholar 

  46. Joët, T., Cournac, L., Peltier, G., and Havaux, M. (2002) Plant Physiol., 128, 760–769.

    Article  PubMed  Google Scholar 

  47. Bendall, D. S., and Manasse, R. S. (1995) Biochim. Biophys. Acta, 1229, 23–38.

    Google Scholar 

  48. Myers, J. (1987) Photosynth. Res., 14, 55–69.

    Google Scholar 

  49. Yu, L., Zhao, J., Mühlenhoff, U., Bryant, D. A., and Golbeck, G. H. (1993) Plant Physiol., 103, 171–180.

  50. Joliot, P., and Joliot, A. (2002) Proc. Natl. Acad. Sci. USA, 99, 10209–10214.

    Article  PubMed  Google Scholar 

  51. Samuilov, V. D., and Fedorenko, T. A. (1999) Biochemistry (Moscow), 64, 610–619.

    Google Scholar 

  52. Takano, M., Takahashi, M.-A., and Asada, K. (1982) Arch. Biochem. Biophys., 218, 369–375.

    PubMed  Google Scholar 

  53. Takahashi, M.-A., and Asada, K. (1976) Eur. J. Biochem., 64, 445–452.

    PubMed  Google Scholar 

  54. Koulougliotis, D., Kostopoulos, T., Petrouleas, V., and Diner, B. A. (1993) Biochim. Biophys. Acta, 1141, 275–282.

    Google Scholar 

  55. Keren, N., Kidd, M. J., Penner-Hahn, J. E., and Pakrasi, H. (2002) Biochemistry, 41, 15085–15092.

    Article  PubMed  Google Scholar 

  56. Samuilov, V. D., Renger, G., Paschenko, V. Z., Oleskin, A. V., Gusev, M. V., Gubanova, O. N., Vasil'ev, S. S., and Barsky, E. L. (1995) Photosynth. Res., 46, 455–465.

    Google Scholar 

  57. Ünnerud, H., Zhang, L., Gellerstedt, G., and Henriksson, G. (2002) Plant Cell, 14, 1953–1962.

    Article  PubMed  Google Scholar 

  58. Bhat, V. B., and Madyastha, K. M. (2001) Biochem. Biophys. Res. Commun., 285, 262–266.

    Article  PubMed  Google Scholar 

  59. Nishiyama, Y., Yamamoto, H., Allakhverdiev, S. I., Inaba, M., Yokota, A., and Murata, N. (2001) EMBO J., 20, 5587–5594.

    Article  PubMed  Google Scholar 

  60. Allakhverdiev, S. I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki, Y., and Murata, N. (2002) Plant Physiol., 130, 1443–1453.

    Article  PubMed  Google Scholar 

  61. Ning, S.-B., Guo, H.-L., Wang, L., and Song, Y.-C. (2002) J. Appl. Microbiol., 93, 15–28.

    Article  PubMed  Google Scholar 

  62. Segovia, M., Haramaty, L., Berges, J. A., and Falkowski, P. G. (2003) Plant Physiol., 132, 99–105.

    Article  PubMed  Google Scholar 

  63. Komissarov, G. G. (1995) Khim. Fiz., 14, 20–28.

    Google Scholar 

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Samuilov, V.D., Timofeev, K.N., Sinitsyn, S.V. et al. H2O2-Induced Inhibition of Photosynthetic O2 Evolution by Anabaena variabilis Cells. Biochemistry (Moscow) 69, 926–933 (2004). https://doi.org/10.1023/B:BIRY.0000040227.66714.19

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  • DOI: https://doi.org/10.1023/B:BIRY.0000040227.66714.19

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