Biochemistry (Moscow)

, Volume 72, Issue 10, pp 1151–1160 | Cite as

Nitrate reductases: Structure, functions, and effect of stress factors

  • E. V. Morozkina
  • R. A. Zvyagilskaya


Structural and functional peculiarities of four types of nitrate reductases are considered: assimilatory nitrate reductase of eukaryotes, as well as cytoplasmic assimilatory, membrane-bound respiratory, and periplasmic dissimilatory bacterial nitrate reductases. Arguments are presented showing that eukaryotic organisms are capable of nitrate dissimilation. Data concerning new classes of extremophil nitrate reductases, whose active center does not contain molybdocofactor, are summarized.

Key words

nitrate reductase nitrification denitrification molybdenum molybdenum cofactor molybdopterin-guanine dinucleotides stress 



dimethyl sulfoxide


eukaryotic assimilatory NRase


molybdopterin-guanine dinucleotide




molybdenum cofactor


periplasmic dissimilatory NRase


membrane-bound respiratory NRase


cytoplasmic assimilatory NRase


nitrate reductase


trimethylamine N-oxide


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  1. 1.
    Campbell, W. H. (1999) Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 277–303.PubMedCrossRefGoogle Scholar
  2. 2.
    Campbell, W. H. (2001) Cell. Mol. Life Sci., 58, 194–204.PubMedCrossRefGoogle Scholar
  3. 3.
    Moreno-Vivian, C., Cabello, P., Martinez-Luque, M., Blasco, R., and Castillo, F. (1999) J. Bacteriol., 181, 6573–6584.PubMedGoogle Scholar
  4. 4.
    Richardson, D. J. (2000) Microbiology, 146, 551–571.PubMedGoogle Scholar
  5. 5.
    Richardson, D. J., Berks, B. C., Russell, D. A., Spiro, S., and Taylor, C. J. (2001) Cell. Mol. Life Sci., 58, 165–178.PubMedCrossRefGoogle Scholar
  6. 6.
    Stolz, J. F., and Basu, P. (2002) ChemBioChem., 3, 198–206.PubMedCrossRefGoogle Scholar
  7. 7.
    Dias, J. M., Than, M. E., Humm, A., Huber, R., Bourenkov, G. P., Bartunik, H. D., Bursakov, S., Calvete, J., Caldeira, J., Carneiro, C., Moura, J. J. G., Moura, I., and Romao, M. J. (1999) Structure Fold Des., 7, 65–79.PubMedCrossRefGoogle Scholar
  8. 8.
    Boyington, J. C., Gladyshev, V. N., Khangulov, S. V., Stadtman, T. C., and Sun, P. D. (1997) Science, 275, 1305–1308.PubMedCrossRefGoogle Scholar
  9. 9.
    Czjzek, M., Dos Santos, J. P., Pommier, J., Giordano, G., Mejean, V., and Haser, R. (1998) J. Mol. Biol., 284, 435–447.PubMedCrossRefGoogle Scholar
  10. 10.
    McAlpine, A. S., McEwan, A. G., and Bailey, S. (1998) J. Mol. Biol., 275, 613–623.PubMedCrossRefGoogle Scholar
  11. 11.
    Butler, C. S., Charnock, J. M., Bennett, B., Sears, H. J., Reilly, A. J., Ferguson, S. J., Garner, C. D., Lowe, D. J., Thomson, A. J., Berks, B. C., and Richardson, D. J. (1999) Biochemistry, 38, 9000–9012.PubMedCrossRefGoogle Scholar
  12. 12.
    Rubio, L. M., Flores, E., and Herrero, A. (1999) FEBS Lett., 462, 358–362.PubMedCrossRefGoogle Scholar
  13. 13.
    Rubio, L. M., Flores, E., and Herrero, A. (2002) Photosynth. Res., 72, 13–26.PubMedCrossRefGoogle Scholar
  14. 14.
    Mikami, B., and Ida, S. (1984) Biochim. Biophys. Acta, 791, 294–304.Google Scholar
  15. 15.
    Blasco, R., Castillo, F., and Martinez-Luque, M. (1997) FEBS Lett., 414, 45–49.PubMedCrossRefGoogle Scholar
  16. 16.
    Lin, J. T., and Stewart, V. (1998) Adv. Microb. Physiol., 38, 1–30.Google Scholar
  17. 17.
    Ogawa, K. I., Akagawa, E., Yamane, K., Sun, Z. W., LaCelle, M., Zuber, P., and Nakano, M. M. (1995) J. Bacteriol., 177, 1409–1413.PubMedGoogle Scholar
  18. 18.
    Lin, J. T., and Stewart, V. (1996) J. Mol. Biol., 256, 423–435.PubMedCrossRefGoogle Scholar
  19. 19.
    Wu, Q., and Stewart, V. (1998) J. Bacteriol., 180, 1311–1322.PubMedGoogle Scholar
  20. 20.
    Ramos, F., Blanco, G., Gutierrez, J. C., Luque, F., and Tortolero, M. (1993) Mol. Microbiol., 8, 1145–1153.PubMedCrossRefGoogle Scholar
  21. 21.
    Frias, J. E., Flores, E., and Herrero, A. (1997) J. Bacteriol., 179, 477–486.PubMedGoogle Scholar
  22. 22.
    Omata, T. (1995) Plant Cell Physiol., 36, 207–213.PubMedGoogle Scholar
  23. 23.
    Moir, J. W., and Wood, N. J. (2001) Cell. Mol. Life Sci., 58, 215–224.PubMedCrossRefGoogle Scholar
  24. 24.
    Deckert, G., Warren, P. V., Gaasterland, T., Young, W. G., Lenox, A. L., Graham, D. E., et al. (1998) Nature, 392, 353–358.PubMedCrossRefGoogle Scholar
  25. 25.
    Kerschen, E. J., Irani, V. R., Hassett, D. J., and Rowe, J. J. (2001) J. Bacteriol., 183, 2125–2131.PubMedCrossRefGoogle Scholar
  26. 26.
    Wu, S. Q., Chai, W., Lin, J. T., and Stewart, V. (1999) J. Bacteriol., 181, 7274–7284.PubMedGoogle Scholar
  27. 27.
    Castillo, F., Dobao, M. M., Reyes, F., Blasco, R., Roldan, M. D., Gavira, M., Caballero, F. J., Moreno-Vivian, C., and Martinez-Luque, M. (1996) Curr. Microbiol., 33, 341–346.PubMedCrossRefGoogle Scholar
  28. 28.
    Herrero, A., Muro-Pastor, A. M., and Flores, E. (2001) J. Bacteriol., 183, 411–425.PubMedCrossRefGoogle Scholar
  29. 29.
    Maeda, S., and Omata, T. (2004) J. Bacteriol., 186, 2107–2114.PubMedCrossRefGoogle Scholar
  30. 30.
    Zumft, W. G. (1997) Microbiol. Mol. Biol. Rev., 61, 533–616.PubMedGoogle Scholar
  31. 31.
    Berks, B. C., Ferguson, S. J., Moir, J. W., and Richardson, D. J. (1995) Biochim. Biophys. Acta, 1232, 97–173.PubMedCrossRefGoogle Scholar
  32. 32.
    Philippot, L., and Hojberg, O. (1999) Biochim. Biophys. Acta, 1446, 1–23.PubMedGoogle Scholar
  33. 33.
    Magalon, A., Rothery, R. A., Giordano, G., Blasco, F., and Weiner, J. H. (1997) J. Bacteriol., 179, 5037–5045.PubMedGoogle Scholar
  34. 34.
    Jormakka, M., Byrne, B., and Iwata, S. (2003) FEBS Lett., 545, 25–30.PubMedCrossRefGoogle Scholar
  35. 35.
    Jepson, B. J., Anderson, L. J., Rubio, L. M., Taylor, C. J., Butler, C. S., Flores, E., Herrero, A., Butt, J. N., and Richardson, D. J. (2004) J. Biol. Chem., 279, 32212–32218.PubMedCrossRefGoogle Scholar
  36. 36.
    Gregory, L. G., Bond, P. L., Richardson, D. J., and Spiro, S. (2003) Microbiology, 149, 229–237.PubMedCrossRefGoogle Scholar
  37. 37.
    Schindelin, H., Kisker, C., Hilton, J., Rajagopalan, K. V., and Rees, D. C. (1996) Science, 14, 1615–1621.CrossRefGoogle Scholar
  38. 38.
    Hille, R., Retey, J., Bartlewski-Hof, V., Reichenbechen, W., and Schink, B. (1999) FEMS Microbiol. Rev., 22, 489–501.CrossRefGoogle Scholar
  39. 39.
    Henikoff, S., and Henikoff, J. G. (1991) Nucleic Acids Res., 19, 6565–6572.PubMedCrossRefGoogle Scholar
  40. 40.
    Khoroshilova, N., Popescu, C., Munck, E., Beinert, H., and Kiley, P. J. (1997) Proc. Natl. Acad. Sci. USA, 94, 6087–6092.PubMedCrossRefGoogle Scholar
  41. 41.
    Hartig, E., Schiek, U., Vollack, K. U., and Zumft, W. G. (1999) J. Bacteriol., 181, 3658–3665.PubMedGoogle Scholar
  42. 42.
    Philippot, L., Mirleau, P., Mazurier, S., Siblot, S., Hartmann, A., Lemanceau, P., and Germon, J. C. (2001) Biochim. Biophys. Acta, 1517, 436–440.PubMedGoogle Scholar
  43. 43.
    Bates, D. M., Lazazzera, B. A., and Kiley, P. J. (1995) J. Bacteriol., 177, 3972–3978.PubMedGoogle Scholar
  44. 44.
    Galimand, M., Gamper, M., Zimmermann, A., and Haas, D. (1991) J. Bacteriol., 173, 1598–1606.PubMedGoogle Scholar
  45. 45.
    Sawers, R. G. (1991) Mol. Microbiol., 5, 1469–1481.PubMedCrossRefGoogle Scholar
  46. 46.
    Ye, R. W., Haas, D., Ka, J. O., Krishnapillai, V., Zimmermann, A., Baird, C., and Tiedje, J. M. (1995) J. Bacteriol., 177, 3606–3609.PubMedGoogle Scholar
  47. 47.
    Berks, B. C., Page, M. D., Richardson, D. J., Reilly, A., Cavill, A., Outen, F., and Ferguson, S. J. (1995) Mol. Microbiol., 15, 319–331.PubMedCrossRefGoogle Scholar
  48. 48.
    Bedzyk, L., Wang, T., and Ye, R. W. (1999) J. Bacteriol., 181, 2802–2806.PubMedGoogle Scholar
  49. 49.
    Butler, C. S., Charnock, J. M., Bennett, B., Sears, H. J., Reilly, A. J., Ferguson, S. J., Garner, C. D., Lowe, D. J., Thomson, A. J., Berks, B. C., and Richardson, D. J. (1999) Biochemistry, 38, 9000–9012.PubMedCrossRefGoogle Scholar
  50. 50.
    Ellington, M. J. K., Sawers, G., Sears, H. J., Spiro, S., Richardson, D. J., and Ferguson, S. J. (2003) Microbiology, 149, 1533–1540.PubMedCrossRefGoogle Scholar
  51. 51.
    Reyes, F., Gavira, M., Castillo, F., and Moreno-Vivian, C. (1998) Biochem. J., 331, 897–904.PubMedGoogle Scholar
  52. 52.
    Gavira, M., Roldan, M. D., Castillo, F., Moreno-Vivian, C. (2002) J. Bacteriol., 184, 1693–1702.PubMedCrossRefGoogle Scholar
  53. 53.
    Siddiqui, R. A., Warnecke-Eberz, U., Hengsberger, A., Schneider, B., and Friedrich, B. (1993) J. Bacteriol., 175, 5867–5876.PubMedGoogle Scholar
  54. 54.
    Bell, L. C., Richardson, D. J., and Ferguson, S. J. (1990) FEBS Lett., 265, 85–87.PubMedCrossRefGoogle Scholar
  55. 55.
    Dobao, M. M., Martinez-Luque, M., Moreno-Vivian, C., and Castillo, F. (1994) Can. J. Microbiol., 40, 645–650.Google Scholar
  56. 56.
    Brondijk, T. H. C., Fiegen, D., Richardson, D. J., and Cole, J. A. (2002) Mol. Microbiol., 44, 245–255.PubMedCrossRefGoogle Scholar
  57. 57.
    Potter, L. C., Millington, P. D., Thomas, G. H., Rothery, R. A., Giordano, G., and Cole, J. (2000) FEMS Microbiol. Lett., 185, 51–57.PubMedCrossRefGoogle Scholar
  58. 58.
    Potter, L., Angove, H., Richardson, D., and Cole, J. A. (2001) Adv. Microb. Physiol., 45, 51–112.PubMedCrossRefGoogle Scholar
  59. 59.
    Carter, J. P., Richardson, D. J., and Spiro, S. (1995) Arch. Microbiol., 163, 159–166.PubMedGoogle Scholar
  60. 60.
    Vollack, K., Xie, J., Hartig, E., Romling, U., and Zumft, W. G. (1998) Microbiology, 144, 441–448.PubMedGoogle Scholar
  61. 61.
    Berks, B. C., Richardson, D. J., Reilly, A., Willis, A. C., and Ferguson, S. J. (1995) Biochem. J., 309, 983–992.PubMedGoogle Scholar
  62. 62.
    Philippot, L., Clays-Josserand, A., Lensi, R., Trinsoutrot, I., Normand, P., and Potier, P. (1997) Biochim. Biophys. Acta, 1350, 272–276.PubMedGoogle Scholar
  63. 63.
    Stewart, V., Lu, Y., and Darwin, A. J. (2002) J. Bacteriol., 184, 1314–1323.PubMedCrossRefGoogle Scholar
  64. 64.
    Flanagan, D. A., Gregory, L. G., Carter, J. P., Karakas-Sen, A., Richardson, D. J., and Spiro, S. (1999) FEMS Microbiol. Lett., 177, 263–270.PubMedCrossRefGoogle Scholar
  65. 65.
    Simon, J., Gross, R., Einsle, O., Kroneck, P. M. H., Kroger, A., and Klimmek, O. (2000) Mol. Microbiol., 35, 686–696.PubMedCrossRefGoogle Scholar
  66. 66.
    Kiley, P. J., and Beinert, H. (1998) FEMS Microbiol. Rev., 22, 341–352.PubMedCrossRefGoogle Scholar
  67. 67.
    Philippot, L. (2002) Biochim. Biophys. Acta, 1577, 355–376.PubMedGoogle Scholar
  68. 68.
    Darwin, A. J., Ziegelhoffer, E. C., Kiley, P. J., and Stewart, V. (1998) J. Bacteriol., 180, 4192–4198.PubMedGoogle Scholar
  69. 69.
    Stewart, V., Bledsoe, P. J., and Williams, S. B. (2003) J. Bacteriol., 185, 5862–5870.PubMedCrossRefGoogle Scholar
  70. 70.
    Wang, H., Tseng, C.-P., and Gunsalus, R. P. (1999) J. Bacteriol., 181, 5303–5308.PubMedGoogle Scholar
  71. 71.
    Sears, H. J., Sawers, G., Reilly, A., Berks, B. C., Ferguson, S. J., and Richardson, D. J. (2000) Microbiology, 146, 2977–2985.PubMedGoogle Scholar
  72. 72.
    Eser, M., and Ehrmann, M. (2003) Proc. Natl. Acad. Sci. USA, 100, 13231–13234.PubMedCrossRefGoogle Scholar
  73. 73.
    Fekkes, P. A., and Driessen, J. M. (1999) Microbiol. Mol. Biol. Rev., 63, 161–173.PubMedGoogle Scholar
  74. 74.
    Dilks, K., Rose, R. W., Hartmann, E., and Pohlschroder, M. (2003) J. Bacteriol., 185, 1478–1483.PubMedCrossRefGoogle Scholar
  75. 75.
    Berks, B. C., Sargent, F., and Palmer, T. (2000) Mol. Microbiol., 35, 260–274.PubMedCrossRefGoogle Scholar
  76. 76.
    Santini, C. L., Ize, B., Chanal, A., Muller, M., Giordano, G., and Wu, L. F. (1998) EMBO J., 17, 101–112.PubMedCrossRefGoogle Scholar
  77. 77.
    Sargent, F., Bogsch, E. G., Stanley, N., Wexler, M., Robinson, C., Berks, B. C., and Palmer, T. (1998) EMBO J., 17, 3640–3650.PubMedCrossRefGoogle Scholar
  78. 78.
    Weiner, J. H., Bilous, P. T., Shaw, G. M., Lubitz, S. P., Frost, L., Thomas, G. H., Cole, J. A., and Turner, R. J. (1998) Cell, 93, 93–101.PubMedCrossRefGoogle Scholar
  79. 79.
    Inokuchi, R., Kuma, K., Miyata, T., and Okada, M. (2002) Physiol. Plant., 116, 1–11.PubMedCrossRefGoogle Scholar
  80. 80.
    Joseph-Horne, T., Hollomon, D. W., and Wood, P. M. (2001) Biochim. Biophys. Acta, 1504, 179–195.PubMedCrossRefGoogle Scholar
  81. 81.
    Siverio, J. M. (2002) FEMS Microbiol. Rev., 26, 277–284.PubMedCrossRefGoogle Scholar
  82. 82.
    Avila, J., Gonzalez, C., Brito, N., Machin, F., Perez, M. D., and Siverio, J. M. (2002) Yeast, 19, 537–544.PubMedCrossRefGoogle Scholar
  83. 83.
    Amaar, Y. G., and Moore, M. M. (1998) Curr. Genet., 33, 206–215.PubMedCrossRefGoogle Scholar
  84. 84.
    Hall, N., and Tomsett, A. B. (2000) Microbiology, 146, 1399–1406.PubMedGoogle Scholar
  85. 85.
    Llamas, A., Igeno, M., Galvan, A., and Fernandez, E. (2002) Plant J., 30, 261–271.PubMedCrossRefGoogle Scholar
  86. 86.
    Zhou, J.-J., Fernandez, E., Galvan, A., and Miller, A. J. (2000) FEBS Lett., 466, 225–227.PubMedCrossRefGoogle Scholar
  87. 87.
    Okamoto, P. M., and Marzluf, G. A. (1993) Mol. Gen. Genet., 240, 221–230.PubMedCrossRefGoogle Scholar
  88. 88.
    Galvan, A., and Fernandez, E. (2001) CMLS, Cell. Mol. Life Sci., 58, 225–233.CrossRefGoogle Scholar
  89. 89.
    Daniel-Vedele, F., Filleur, S., and Caboche, M. (1998) Curr. Opin. Plant Biol., 1, 235–239.PubMedCrossRefGoogle Scholar
  90. 90.
    Forde, B. (2000) Biochim. Biophys. Acta, 1465, 219–235.PubMedCrossRefGoogle Scholar
  91. 91.
    Crawford, N. M., and Glass, A. M. D. (1998) Trends Plant Sci., 3, 389–395.CrossRefGoogle Scholar
  92. 92.
    Pao, S. S., Paulsen, I. T., and Saier, M. H. (1998) Microbiol. Mol. Biol. Rev., 62, 1–34.PubMedGoogle Scholar
  93. 93.
    Takaya, N. (20020 J. Biosci. Bioeng., 94, 506–510.Google Scholar
  94. 94.
    Shoun, H., Kim, D.-H., Uchiyama, H., and Sugiyama, J. (1992) FEMS Microbiol. Lett., 94, 277–282.CrossRefGoogle Scholar
  95. 95.
    Tsuruta, S., Takaya, N., Zhang, L., Shoun, H., Kimura, K., Hamamoto, M., and Nakase, T. (1998) FEMS Microbiol. Lett., 168, 105–110.PubMedCrossRefGoogle Scholar
  96. 96.
    Watsuji, T., Takaya, N., Nakamura, A., and Shoun, H. (2003) Biosci. Biotech. Biochem., 67, 1115–1120.CrossRefGoogle Scholar
  97. 97.
    Zhou, Z., Takaya, N., Nakamura, A., Yamaguchi, M., Takeo, K., and Shoun, H. (2002) J. Biol. Chem., 277, 1892–1896.PubMedCrossRefGoogle Scholar
  98. 98.
    Takaya, N., Kuwazaki, S., Adachi, Y., Suzuki, S., Kikuchi, T., Nakamura, H., Shiro, Y., and Shoun, H. (2003) J. Biochem., 133, 461–465.PubMedCrossRefGoogle Scholar
  99. 99.
    Kobayashi, M., Matsuo, Y., Takimoto, A., Suzuki, S., Maruo, F., and Shoun, H. (1996) J. Biol. Chem., 271, 16263–16267.PubMedCrossRefGoogle Scholar
  100. 100.
    Kurakov, A. V., Nosikov, A. N., Skrynnikova, E. V., and L’vov, N. P. (2000) Curr. Microbiol., 41, 114–119.PubMedCrossRefGoogle Scholar
  101. 101.
    Uchimura, H., Enjoji, H., Seki, T., Taguchi, A., Takaya, N., and Shoun, H. (2002) J. Biochem., 131, 579–586.PubMedGoogle Scholar
  102. 102.
    Volkl, P., Huber, R., Drobner, E., Rachel, R., Burggraf, S., Trincone, A., et al. (1993) Appl. Environ. Microbiol., 59, 2918–2926.PubMedGoogle Scholar
  103. 103.
    Tomlinson, G. A., Jahnke, L. L., and Hochstein, L. I. (1986) Int. J. Syst. Bacteriol., 36, 66–70.PubMedCrossRefGoogle Scholar
  104. 104.
    Ramirez-Arcos, S., Fernandez-Herrero, L. A., and Berenguer, J. (1998) Biochim. Biophys. Acta, 1396, 215–227.PubMedGoogle Scholar
  105. 105.
    Miroshnichenko, M. L., Kostrikina, N. A., Chernyh, N. A., Pimenov, N. V., Tourova, T. P., Antipov, A. N., Spring, S., Stackebrandt, E., and Bonch-Osmolovskaya, E. A. (2003) Int. J. Syst. Evol. Microbiol., 53, 323–329.PubMedCrossRefGoogle Scholar
  106. 106.
    Vetriani, C., Speck, M. D., Ellor, S. V., Lutz, R. A., and Starovoytov, V. (2004) Int. J. Syst. Evol. Microbiol., 54, 175–181.PubMedCrossRefGoogle Scholar
  107. 107.
    Afshar, S., Kim, C., Monbouquette, H. G., and Schroder, I. (1998) Appl. Environ. Microbiol., 64, 3004–3008.PubMedGoogle Scholar
  108. 108.
    Yoshimatsu, K., Sakurai, T., and Fujiwara, T. (2000) FEBS Lett., 470, 216–220.PubMedCrossRefGoogle Scholar
  109. 109.
    Hochstein, L. I., and Lang, F. (1991) Arch. Biochem. Biophys., 288, 380–385.PubMedCrossRefGoogle Scholar
  110. 110.
    Afshar, S., Johnson, E., de Vries, S., and Schroder, I. (2000) J. Bacteriol., 183, 5491–5495.CrossRefGoogle Scholar
  111. 111.
    Hille, R. (2002) Trends Biochem. Sci., 27, 360–367.PubMedCrossRefGoogle Scholar
  112. 112.
    L’vov, N. P., Nosikov, A. N., and Antipov, A. N. (2002) Biochemistry (Moscow), 67, 196–200.CrossRefGoogle Scholar
  113. 113.
    Morozkina, E. V., Nosikov, A. N., Zvyagilskaya, R. A., and L’vov, N. P. (2005) Biochemistry (Moscow), 70, 809–814.CrossRefGoogle Scholar
  114. 114.
    Nosikov, A. N., Chichikalo, E. V., Golubeva, L. I., Zvyagilskaya, R. A., and L’vov, N. P. (2000) Biochemistry (Moscow), 65, 204–207.Google Scholar
  115. 115.
    Antipov, A. N., Lyalikova, N. N., Khijniak, T. V., and L’vov, N. P. (1998) FEBS Lett., 441, 257–260.PubMedCrossRefGoogle Scholar
  116. 116.
    Murillo, M. F., Gugliuzza, T., Senko, J., Basu, P., and Stolz, J. F. (1999) Arch. Microbiol., 172, 313–320.CrossRefGoogle Scholar
  117. 117.
    Antipov, A. N., Morozkina, E. V., Sorokin, D. Yu., Golubeva, L. B., Zvyagilskaya, R. A., and L’vov, N. P. (2005) Biochemistry (Moscow), 70, 799–803.CrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2007

Authors and Affiliations

  1. 1.Bach Institute of BiochemistryRussian Academy of SciencesMoscowRussia

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