Abstract
Closely related penta- and octaheme nitrite reductases catalyze the reduction of nitrite, nitric oxide, and hydroxylamine to ammonium and of sulfite to sulfide. NrfA pentaheme nitrite reductase plays the key role in anaerobic nitrate respiration and the protection of bacterial cells from stresses caused by nitrogen oxides and hydrogen peroxide. Octaheme nitrite reductases from bacteria of the Thioalkalivibrio genus are less studied, and their function in the cell is unknown. In order to estimate the possible role of octaheme nitrite reductases in the cell resistance to oxidative stress, the peroxidase activity of the enzyme from T. nitratireducens (TvNiR) has been studied in detail. Comparative analysis of the active site structure of TvNiR and cytochrome c peroxidases has shown some common features, such as a five-coordinated catalytic heme and identical catalytic residues in active sites. A model of the possible productive binding of peroxide at the active site of TvNiR has been proposed. The peroxidase activity has been measured for TvNiR hexamers and trimers under different conditions (pH, buffers, the addition of CaCl2 and EDTA). The maximum peroxidase activity of TvNiR with ABTS as a substrate (k cat = 17 s–1; k cat/K m = 855 mM–1 s–1) has been 100–300 times lower than the activity of natural peroxidases. The different activities of TvNiR trimers and hexamers indicate that the rate-limiting stage of the reaction is not the catalytic event at the active site but the electron transfer along the heme c electron-transport chain.
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References
Simon, J., FEMS Microbiol. Rev., 2002, vol. 26, pp. 285–309.
Einsle, O., Methods. Enzymol., 2011, vol. 496, pp. 399–422.
Einsle, O., Messerschmidt, A., Stach, P., Bourenkov, G.P., Bartunik, H.D., Huber, R., and Kroneck, P.M.H., Nature, 1999, vol. 400, no. 6743, pp. 476–480.
Clarke, T.A., Mills, P.C., Poock, S.R., Butt, J.N., Cheesman, M.R., Cole, J.A., Hinton, J.C., Hemmings, A.M., Kemp, G., Soderberg, C.A., Spiro, S., van Wonderen, J., and Richardson, D.J., Methods Enzymol., 2008, vol. 437, pp. 63–77.
Tikhonova, T., Tikhonov, A., Trofimov, A., Polyakov, K., Boyko, K., Cherkashin, E., Rakitina, T., Sorokin, D., and Popov, V., FEBS J., 2012, vol. 279, no. 21, pp. 4052–4061.
Tikhonova, T.V., Trofimov, A.A., and Popov, V.O., Biochemistry (Moscow), 2012, vol. 77, no. 10, pp. 1129–1138.
Einsle, O., Stach, P., Messerschmidt, A., Simon, J., Kroger, A., Huber, R., and Kroneck, P.M.H., J. Biol. Chem., 2000, vol. 275, pp. 39608–39616.
Bamford, V.A., Angove, H.C., Seward, H.E., Thomson, A.J., Cole, J.A., Butt, J.N., Hemmings, A.M., and Richardson, D.J., Biochemistry, 2002, vol. 41, pp. 2921–2931.
Lockwood, C.W., Burlat, B., Cheesman, M.R., Kern, M., Simon, J., Clarke, T.A., Richardson, D.J., and Butt, J.N., J. Am. Chem. Soc., 2015, vol. 137, no. 8, pp. 3059–3068.
Cunha, C.A., Macieira, S., Dias, J.M., Almeida, G., Goncalves, L.L., Costa, C., Lampreia, J., Huber, R., Moura, J.J.G., Moura, I., and Romao, M.J., J. Biol. Chem., 2003, vol. 278, pp. 17455–17465.
Rodrigues, M.L., Oliveira, T.F., Pereira, I.A.C., and Archer, M., EMBO J., 2006, vol. 25, pp. 5951–5960.
Youngblut, M., Judd, E.T., Srajer, V., Sayyed, B., Goelzer, T., Elliott, S.J., Schmidt, M., and Pacheco, A.A., J. Biol. Inorg. Chem., 2012, vol. 17, pp. 647–662.
Kemp, G.L., Clarke, T.A., Marritt, S.J., Lockwood, C., Poock, S.R., Hemmings, A.M., Richardson, D.J., Cheesman, M.R., and Butt, J.N., Biochem. J., 2010, vol. 431, no. 1, pp. 73–80.
van Wonderen, J.H., Burlat, B., Richardson, D.J., Cheesman, M.R., and Butt, J.N., J. Biol. Chem., 2008, vol. 283, no. 15, pp. 9587–9594.
Angove, H.C., Cole, J.A., Richardson, D.J., and Butt, J.N., J. Biol. Chem., 2002, vol. 277, pp. 23374–23381.
Lukat, P., Rudolf, M., Stach, P., Messerschmidt, A., Kroneck, P.M., Simon, J., and Einsle, O., Biochemistry, 2008, vol. 47, no. 7, pp. 2080–2086.
Rudolf, M., Einsle, O., Neese, F., and Kroneck, P.M., Biochem. Soc. Trans., 2002, vol. 30, no. 4, pp. 649–653.
Kern, M., Volz, J., and Simon, J., Environ. Microbiol., 2011, vol. 13, no. 9, pp. 2478–2494.
Muhlig, A., Kabisch, J., Pichner, R., Scherer, S., and Muller-Herbst, S., Food Microbiol., 2014, vol. 42, pp. 26–33.
Pittman, M.S., Elvers, K.T., Lee, L., Jones, M.A., Poole, R.K., Park, S.F., and Kelly, D.J., Mol. Microbiol., 2007, vol. 63, pp. 575–590.
Tikhonova, T.V., Slutsky, A., Antipov, A.N., Boyko, K.M., Polyakov, K.M., Sorokin, D.Y., Zvyagilskaya, R.A., and Popov, V.O., Biochim. Biophys. Acta, 2006, vol. 1764, pp. 715–723.
Polyakov, K.M., Boyko, KM., Tikhonova, T.V., Slutsky, A., Antipov, A.N., Zvyagilskaya, R.A., Popov, A.N., Bourenkov, G.P., Lamzin, V.S., and Popov, V.O., J. Mol. Biol., 2009, vol. 389, pp. 846–862.
Sorokin, D.Y., Tourova, T.P., Sjollema, K.A., and Kuenen, J.G., Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 1779–1783.
Sorokin, D.Y., Antipov, A.N., and Kuenen, J.G., Arch. Microbiol., 2003, vol. 180, pp. 127–133.
Sorokin, D.Y., Tourova, T.P., Lysenko, A.M., Mityushina, L.L., and Kuenen, J.G., Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 657–664.
Tikhonova, T.V., Slutskaya, E.S., Filimonenkov, A.A., Boiko, K.M., Kleimenov, S.Yu., Konarev, P.V., Polyakov, K.M., Svergun, D.I., Trofimov, A.A., Khomenkov, V.G., Zvyagil’skaya, R.A., and Popov, V.O., Biochemistry (Moscow), 2008, vol. 73, no. 2, pp. 164–170.
Yamada, S., Suruga, K., Ogawa, M., Hama, T., Satoh, T., Kawachi, R., Nishio, T., and Oku, T., Biosci. Biotechnol. Biochem., 2002, vol. 66, no. 10, pp. 2044–2051.
Prasad, S., Maiti, N.C., Mazumdar, S., and Mitra, S., Biochim. Biophys. Acta, 2002, vol. 1596, pp. 63–75.
Suruga, K., Murakami, K., Taniyama, Y., Hama, T., Chida, H., Satoh, T., Yamada, S., Hakamata, W., Kawachi, R., Isogai, Y., Nishio, T., and Oku, T., Biochem. Biophys. Res. Commun., 2004, vol. 315, no. 4, pp. 815–822.
Poulos, T.L., Freer, S.T., Alden, R.A., Edwards, S.L., Skogland, U., Takio, K., Eriksson, B., Xuong, N., Yonetani, T., and Kraut, J., J. Biol. Chem., 1980, vol. 255, no. 2, pp. 575–580.
Poulos, T.L., Curr. Opin. Biotechnol, 1993, vol. 4, no. 4, pp. 484–489.
Choudhury, K., Sundaramoorthy, M., Hickman, A., Yonetani, T., Woehl, E., Dunn, M.F., and Poulos, T.L., J. Biol. Chem., 1994, vol. 269, no. 32, pp. 20239–20249.
Kunishima, N., Fukuyama, K., Matsubara, H., Hatanaka, H., Shibano, Y., and Amachi, T., J. Mol. Biol., 1994, vol. 235, no. 1, pp. 331–344.
Schuller, D.J., Ban, N., Huystee, R.B., McPherson, A., and Poulos, T.L., Structure, 1996, vol. 4, pp. 311–321.
Gajhede, M., Schuller, D.J., Henriksen, A., Smith, A.T., and Poulos, T.L., Nat. Struct. Biol., 1997, vol. 4, pp. 1032–1038.
Erman, J.E. and Vitello, L.B., Biochim. Biophys. Acta, 2002, vol. 1597, pp. 193–220.
Finzel, B.C., Poulos, T.L., and Kraut, J., J. Biol. Chem., 1984, vol. 259, pp. 13027–13036.
Gazaryan, I.G., Khushpul’yan, D.M., and Tishkov, V.I., Usp. Biol. Khim., 2006, vol. 46, pp. 303–322.
Trofimov, A.A., Polyakov, K.M., Boiko, K.M., Filimonenkov, A.A., Dorovatovskii, P.V., Tikhonova, T.V., Popov, V.O., and Koval’chuk, M.V., Kristallografiya, 2010, vol. 55, no. 10, pp. 1176–1182.
Einsle, O., Messerschmidt, A., Huber, R., Kroneck, P.M., and Neese, F., J. Am. Chem. Soc., 2002, vol. 124, no. 39, pp. 11737–11745.
Kamal, J.K. and Behere, D.V., J. Inorg. Biochem., 2003, vol. 94, no. 3, pp. 236–242.
Radi, R., Thomson, L., Rubbo, H., and Prodanov, E., Arch. Biochem. Biophys., 1991, vol. 288, pp. 112–117.
Sakharov, I.Y., Biochemistry (Moscow), 2001, vol. 66, no. 1, pp. 515–519.
Chen, Y., Lykourinou, V., Hoang, T., Ming, L.-J., and Ma, S., Inorg. Chem., 2012, vol. 51, pp. 12600–12602.
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Original Russian Text © T.V. Tikhonova, E.S. Slutskaya, V.O. Popov, 2017, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2017, Vol. 53, No. 2, pp. 155–163.
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Tikhonova, T.V., Slutskaya, E.S. & Popov, V.O. Peroxidase activity of octaheme nitrite reductases from bacteria of the Thioalkalivibrio genus. Appl Biochem Microbiol 53, 157–164 (2017). https://doi.org/10.1134/S0003683817020168
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DOI: https://doi.org/10.1134/S0003683817020168