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The Production of Ammonia by Multiheme Cytochromes c

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The Metal-Driven Biogeochemistry of Gaseous Compounds in the Environment

Part of the book series: Metal Ions in Life Sciences ((MILS,volume 14))

Abstract

The global biogeochemical nitrogen cycle is essential for life on Earth. Many of the underlying biotic reactions are catalyzed by a multitude of prokaryotic and eukaryotic life forms whereas others are exclusively carried out by microorganisms. The last century has seen the rise of a dramatic imbalance in the global nitrogen cycle due to human behavior that was mainly caused by the invention of the Haber-Bosch process. Its main product, ammonia, is a chemically reactive and biotically favorable form of bound nitrogen. The anthropogenic supply of reduced nitrogen to the biosphere in the form of ammonia, for example during environmental fertilization, livestock farming, and industrial processes, is mandatory in feeding an increasing world population. In this chapter, environmental ammonia pollution is linked to the activity of microbial metalloenzymes involved in respiratory energy metabolism and bioenergetics. Ammonia-producing multiheme cytochromes c are discussed as paradigm enzymes.

Please cite as: Met. Ions Life Sci. 14 (2014) 211–236

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References

  1. M. Rudolf, P. M. H. Kroneck, Met. Ions Biol. Syst. 2005, 43, 75–103.

    CAS  PubMed  Google Scholar 

  2. J. Rockström, W. Steffen, K. Noone, Å. Persson, F. S. Chapin, E. F. Lambin, T. M. Lenton, M. Scheffer, C. Folke, H. J. Schellnhuber, B. Nykvist, C. A. de Wit, T. Hughes, S. van der Leeuw, H. Rodhe, S. Sörlin, P. K. Snyder, R. Costanza, U. Svedin, M. Falkenmark, L. Karlberg, R. W. Corell, V. J. Fabry, J. Hansen, B. Walker, D. Liverman, K. Richardson, P. Crutzen, J. A. Foley, Nature 2009, 461, 472 –475.

    Article  PubMed  Google Scholar 

  3. L. B. Maia, J. J. G. Moura, Chem. Rev. 2014, 114, 5273–5357.

    Google Scholar 

  4. J. A. Brandes, A. H. Devol, C. Deutsch, Chem. Rev. 2007, 107, 577–589.

    Article  CAS  PubMed  Google Scholar 

  5. P. G. Falkowsky, Nature 2007, 387, 272–275.

    Article  Google Scholar 

  6. J. N. Galloway, F. J. Dentener, D. G. Capone, E. W. Boyer, R. W. Howarth, S. P. Seitzinger, G. P. Asner, C. C. Cleveland, P. A. Green, E. A. Holland, D. M. Karl, A. F. Michaels, J. H. Porter, A. R. Townsend, C. J. Vörösmarty, Biogeochemistry 2004, 70,153–226.

    Article  CAS  Google Scholar 

  7. Sustaining Life on Planet Earth: Metalloenzymes Mastering Dioxygen and Other Chewy Gases, Eds P. M. H. Kroneck, M. E. Sosa Torres; Vol. 15 of Metal Ions in Life Sciences; Eds A. Sigel, H. Sigel, R. K. O. Sigel; Springer International Publishing AG, Cham, Switzerland, 2015.

    Google Scholar 

  8. D. K. Newman, J. F. Banfield, Science 2002, 296, 1071–1077.

    Article  CAS  PubMed  Google Scholar 

  9. A. L. Reysenbach, E. Shock, Science 2002, 296, 1077–1082.

    Article  CAS  PubMed  Google Scholar 

  10. M. Strous, J. A. Fuerst, E. H. Kramer, S. Logemann, G. Muyzer, K. T. van de Pas-Schoonen, R. Webb, J. G. Kuenen, M. S. Jetten, Nature 1999, 400, 446–449.

    Article  CAS  PubMed  Google Scholar 

  11. A. H. Devol, Nature 2003, 422, 575–576.

    Article  CAS  PubMed  Google Scholar 

  12. C. R. Penton, A. H. Devol, J. M. Tiedje, Appl. Environ. Microbiol. 2006, 72, 6829–6832.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. M. Ali, L.-Y. Chai, C.-J. Tang, P. Zheng, X.-B. Min, Z.-H. Yang, L. X., Y.-X. Song, Biomed. Res. Int. 2013, doi: 10.1155/2013/134914

  14. B. Kartal, W. J. Maalcke, N. M. de Almeida, I. Cirpus, J. Gloerich, W. Geerts, H. J. M. Op den Camp, H. R. Harhangi, E. M. Janssen-Megens, K.-J. Francoijs, H. G. Stunnenberg, J. T. Keltjens, M. S. M. Jetten, M. Strous, Nature 2011, 479,127–130.

    Article  CAS  PubMed  Google Scholar 

  15. C. Deutsch, J. L. Sarmiento, D. M. Sigman, N. Gruber, J. P. Dunne, Nature 2007, 445, 163–167.

    Article  CAS  PubMed  Google Scholar 

  16. D. G. Capone, A. N. Knapp, Nature 2007, 445, 159–160.

    Article  CAS  PubMed  Google Scholar 

  17. B. B. Ward, Science 2013, 341, 352–353.

    Article  CAS  PubMed  Google Scholar 

  18. D. J. Richardson, Cell. Mol. Life Sci. 2001, 58, 165–178.

    Article  CAS  PubMed  Google Scholar 

  19. J. Simon, FEMS Microbiol. Rev. 2002, 26, 285–309.

    Article  CAS  PubMed  Google Scholar 

  20. O. Einsle, P. M. H. Kroneck, Biol. Chem. 2004, 385, 875–883.

    Article  CAS  PubMed  Google Scholar 

  21. G. Fritz, O. Einsle, M. Rudolf, A. Schiffer, P. M. H. Kroneck, J. Mol. Microbiol. Biotechnol. 2005, 10, 223–233.

    Article  CAS  PubMed  Google Scholar 

  22. M. Kern, J. Simon, Biochim. Biophys. Acta 2009, 1787, 646–656.

    Article  CAS  PubMed  Google Scholar 

  23. J. Simon, M. Kern, B. Hermann, O. Einsle, J. N. Butt, Biochem. Soc. Trans. 2011, 39, 1864–1870.

    Article  CAS  PubMed  Google Scholar 

  24. J. Simon, M. G. Klotz, Biochim. Biophys. Acta 2013, 1827, 114–135.

    Article  CAS  PubMed  Google Scholar 

  25. J. Simon, P. M. H. Kroneck, Adv. Microbial Physiol. 2013, 62, 45–117.

    Article  CAS  Google Scholar 

  26. J. E. Huheey, E. A. Keiter, R. L. Keiter, Inorganic Chemistry: Principles of Structure and Reactivity, 4th edn, HarperCollins College Publishers, 1993, pp. 405–408.

    Google Scholar 

  27. E. Housecroft, A. G. Sharpe, Inorganic Chemistry, 3rd edn, Pearson, Edinburgh Gate, Harlow, UK, 2008, pp. 433–455.

    Google Scholar 

  28. R. A. Alderden, M. D. Hall, T. W. Hambley, J. Chem. Ed. 2006, 83, 728–734.

    Article  CAS  Google Scholar 

  29. S.N. Behera, M. Sharma, V. P. Aneja, R. Balasubramanian, Environ. Sci. Pollut. Res. 2013, 20, 8092–8131.

    Article  CAS  Google Scholar 

  30. M. A. Sutton, S. Reis, S. N. Riddick, U. Dragosits, E. Nemitz, M. R.Theobald, Y. S. Tang, C. F. Braban, M. Vieno, A. J. Dore, R. F. Mitchell, S. Wanless, F. Daunt, D. Fowler, T. D. Blackall, C. Milford, C. R. Flechard, B. Loubet, R. Massad, P. Cellier, E. Personne, P. F. Coheur, L. Clarisse, M. Van Damme, Y. Ngadi, C. Clerbaux, C. A. Skjøth, C. Geels, O. Hertel, R.J. Wichink Kruit, R. W. Pinder, J. O. Bash, J. T. Walker, D. Simpson, L. Horváth, T. H. Misselbrook, A. Bleeker, F. Dentener, W. de Vries, Phil. Trans. R. Soc. B 2013, 368, 20130166; doi: 10.1098/rstb.2013.0166.

  31. Ammonia Gas Monitoring Network (AMoN), within the US National Atmospheric Deposition Program (http://nadp.sws.uiuc.edu/AMoN/).

  32. L. Myles, Nat. Geosci. 2009, 2, 461–462.

    Article  CAS  Google Scholar 

  33. S. Singh, B. R. Bakshi, Environ. Sci. Technol. 2013, 47, 9388–9396.

    Article  CAS  PubMed  Google Scholar 

  34. M. Van Damme, L. Clarisse, C. L. Heald, D. Hurtmans, Y. Ngadi, C. Clerbaux, A. J. Dolman, J. W. Erisman, P. F. Coheur, Atmos. Chem. Phys. Discuss. 2013, 13, 24301–24342.

    Article  Google Scholar 

  35. A. Bytnerowicz, P. E. Padgett, S. D. Parry, M. E. Fenn, M. J. Arbaugh, The Scientific World 2001, 1(S2), 304–311.

    Article  Google Scholar 

  36. B. Gu, J. Chang, Y. Min, Y. Ge, Q. Zhu, J. N. Galloway, C. Peng, Scientific Reports 2013, 3, 2579, 1–7, doi: 10.1038/srep02579.

  37. R. K. Thauer, K. Jungermann, K. Decker, Bacteriol. Rev. 1977, 41, 100–180.

    CAS  PubMed Central  PubMed  Google Scholar 

  38. B. Kartal, N. M. de Almeida, W. J. Maalcke, H. J.M. Op den Camp, M. S. M. Jetten, J. T. Keltjens, FEMS Microbiol. Rev. 2013, 37, 428–461.

    Article  CAS  PubMed  Google Scholar 

  39. T. Fujita, J. Biochem. (Tokyo) 1966, 60, 204–215.

    Google Scholar 

  40. T. Brittain, R. Blackmore, C. Greenwood, A. J. Thomson, Eur. J. Biochem. 1992, 209, 793–802.

    Article  CAS  PubMed  Google Scholar 

  41. W. Schumacher, F. Neese, U. H. Hole, P. M. H. Kroneck, in Transition Metals in Microbial Metabolism, Eds G. Winkelmann, C. J. Carrano, Harwood Academic, Amsterdam, NL, 1997, pp. 329–356.

    Google Scholar 

  42. O. Einsle, Meth. Enzymol. 2011, 496, 399–422.

    Article  CAS  PubMed  Google Scholar 

  43. J. A. Cole, FEMS Microbiol. Lett. 1996, 136, 1–11.

    Article  CAS  PubMed  Google Scholar 

  44. A. Welsh, J. C. Chee-Sanford, L. M. Connor, F. E. Löffler, R. A. Sanford, Appl. Environ. Microbiol. 2014, 80, 2110–2119.

    Article  PubMed Central  PubMed  Google Scholar 

  45. K. Heylen, J. Keltjens, Front. Microbiol. 2012, 3, article 371, 1–27, doi: 10.3389/fmicb.2012.00371.

  46. D. Mania, K. Heylen, R. J. M. van Spanning, Å. Frostegard, Environ. Microbiol. 2014, in press, doi: 10.1111/1462–2920.12478.

  47. B. Strehlitz, B. Gründig, W. Schumacher, P. M. H. Kroneck, K.-D. Vorlop, H. Kotte, Anal. Chem. 1996, 68, 807–816.

    Google Scholar 

  48. J. Tan, J. A. Cowan, Biochemistry 1991, 30, 8910–8917.

    Article  CAS  PubMed  Google Scholar 

  49. M. Rudolf, O. Einsle, F. Neese, P. M. H. Kroneck, Biochem. Soc. Trans. 2002, 30, 649–653.

    Article  CAS  PubMed  Google Scholar 

  50. A. Darwin, H. Hussain, L. Griffiths, J. Grove, Y. Sambongi, S. Busby, J. Cole, Mol. Microbiol. 1993, 9, 1255–1265.

    Article  CAS  PubMed  Google Scholar 

  51. W. Schumacher, P. M. H. Kroneck, Arch. Microbiol. 1991, 156, 70–74.

    Article  CAS  Google Scholar 

  52. M.-C. Liu, H. D. Peck, Jr., J. Biol. Chem. 1981, 256, 13159–13164.

    CAS  PubMed  Google Scholar 

  53. M.-C. Liu, M.-Y. Liu, W. J. Payne, H. D. Peck, Jr., J. Le Gall, D. V. DerVartanian, FEBS Lett. 1987, 218, 227–230.

    Article  CAS  PubMed  Google Scholar 

  54. W. Schumacher, U. H. Hole, P. M. H. Kroneck, Biochem. Biophys. Res. Commun. 1994, 205, 911–916.

    Article  CAS  PubMed  Google Scholar 

  55. G. W. Pettigrew, G. R. Moore, Cytochromes c. Biological Aspects, Springer-Verlag, Berlin, Heidelberg, New York, London, Paris, Tokyo, 1987.

    Book  Google Scholar 

  56. P. M. Wood, Biochim. Biophys. Acta 1984, 768, 293–317.

    Article  CAS  PubMed  Google Scholar 

  57. S. I. Adachi, S. Nagano, K. Ishimori, Y. Watanabe, I. Morishima, T. Egawa, T. Kitagawa, R. Makino, Biochemistry 1993, 32, 241–252.

    Article  CAS  PubMed  Google Scholar 

  58. O. Einsle, A. Messerschmidt, P. Stach, G. P. Bourenkov, H. D. Bartunik, R. Huber, P. M. H. Kroneck, Nature 1999, 400, 476–480.

    Article  CAS  PubMed  Google Scholar 

  59. O. Einsle, P. Stach, A. Messerschmidt, J. Simon, A. Kröger, R. Huber, P. M. H. Kroneck, J. Biol. Chem. 2000, 275, 39608–39616.

    Article  CAS  PubMed  Google Scholar 

  60. V. A. Bamford, H. C. Angove, H. E. Seward, A. J. Thomson, J. Cole, J. N. Butt, A. M. Hemmings, D. J. Richardson, Biochemistry 2002, 41, 2921–2931.

    Article  CAS  PubMed  Google Scholar 

  61. C. A. Cunha, S. Macieira, J. M. Dias, G. Almeida, L. L. Goncalves, C. Costa, J. Lampreia, R. Huber, J. J. G. Moura, I. Moura, M. J. Romao, J. Biol. Chem. 2003, 278, 17455–17465.

    Article  CAS  PubMed  Google Scholar 

  62. M. G. Almeida, S. Macieira, L. L. Goncalves, R. Huber, C. A. Cunha, M. J. Romao, C. Costa, J. Lampreia, J. J. G. Moura, I. Moura, Eur. J. Biochem. 1993, 270, 3904–3915.

    Article  Google Scholar 

  63. M. L. Rodrigues, T. F. Oliveira, I. A. Pereira, M. Archer, EMBO J. 2006, 25, 5951–5960.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. M. Youngblut, E. T. Judd, V. Srajer, B. Sayyed, T. Goelzer, S. J. Elliot, M. Schmidt, A. A. Pacheco, J. Biol. Inorg. Chem. 2012, 17, 647–662.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. M. Kern, F. Eisel, J. Scheithauer, R. G. Kranz, J. Simon, Mol. Microbiol. 2010, 75, 122–137.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. O. Einsle, A. Messerschmidt, R. Huber, P.M.H. Kroneck, F. Neese, J. Am. Chem. Soc. 2002, 124, 11737–11745.

    Article  CAS  PubMed  Google Scholar 

  67. D. Bykov, F. Neese, J. Biol. Inorg. Chem. 2011, 16, 417–430.

    Article  CAS  PubMed  Google Scholar 

  68. D. Bykov, F. Neese, J. Biol. Inorg. Chem. 2012, 17, 741–760.

    Article  CAS  PubMed  Google Scholar 

  69. D. Bykov, M. Plog, F. Neese, J. Biol. Inorg. Chem. 2014, 19, 97–112.

    Article  CAS  PubMed  Google Scholar 

  70. P. Stach, O. Einsle, W. Schumacher, E. Kurun, P. M. H. Kroneck, J. Inorg. Biochem. 2000, 79, 381–385.

    Article  CAS  PubMed  Google Scholar 

  71. T. A. Clarke, A. Hemmings, B. Burlat, J. N. Butt, J. A. Cole, D. J. Richardson, Biochem. Soc. Trans. 2006, 34,143– 145.

    Article  CAS  PubMed  Google Scholar 

  72. P. Lukat, R. Rudolf, P. Stach, A. Messerschmidt, P. M. H. Kroneck, J. Simon, O. Einsle, Biochemistry 2008, 47, 2080–2086.

    Article  CAS  PubMed  Google Scholar 

  73. J. Simon, R. Gross, O. Einsle, P. M. H. Kroneck, A. Kröger, O. Klimmek, Mol. Microbiol. 2000, 35, 686–696.

    Article  CAS  PubMed  Google Scholar 

  74. J. Simon, R. Pisa, T. Stein, R. Eichler, O. Klimmek, R. Gross, Eur. J. Biochem. 2001, 268, 5776–5782.

    Article  CAS  PubMed  Google Scholar 

  75. R. Gross, R. Eichler, J. Simon, Biochem. J. 2005, 390, 689–693.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. J. Simon, in Nitrogen Cycling in Bacteria. Molecular Analysis, Ed J. W. B. Moir, Caister Academic Press, Norfolk, UK, 2011, pp. 39–58

    Google Scholar 

  77. J. Simon, R. J. M. van Spanning, D. J. Richardson, Biochim. Biophys. Acta 2008, 1777, 1480–1490.

    Article  CAS  PubMed  Google Scholar 

  78. H. Hussain, J. Grove, L. Griffiths, S. Busby, J. Cole, Mol. Microbiol. 1994, 12, 153–163.

    Article  CAS  PubMed  Google Scholar 

  79. B. C. Berks, S. J. Ferguson, J. W. B. Moir, D. J. Richardson, Biochim. Biophys. Acta 1995, 1232, 97–173.

    Article  PubMed  Google Scholar 

  80. J. Simon, M. Kern, Biochem. Soc. Trans. 2008, 36, 1011–1016.

    Article  CAS  PubMed  Google Scholar 

  81. M. Jormakka, K. Yokoyama, T. Yano, M. Tamakoshi, S. Akimoto, T. Shimamura, P. Curmi, S. Iwata, Nat. Struct. Mol. Biol. 2008, 15, 730–737.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. T. A. Clarke, J. A. Cole, D. J. Richardson, A. M. Hemmings, Biochem. J. 2007, 406, 19–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. F. Grein, A. R. Ramos, S. S. Venceslau, I. A. C. Pereira, Biochim. Biophys. Acta 2013, 1827, 145–160.

    Article  CAS  PubMed  Google Scholar 

  84. R. G. Kranz, C. Richard-Fogal, J. S. Taylor, E. R. Frawley, Microbiol. Mol. Biol. Rev. 2009, 73, 510–528.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. D. J. Eaves, J. Grove, W. Staudenmann, P. James, R. K. Poole, S. A. White, I. Griffiths, J. A. Cole, Mol. Microbiol. 1998, 28, 205–216.

    Article  CAS  PubMed  Google Scholar 

  86. R. Pisa, T. Stein, R. Eichler, R. Gross, J. Simon, Mol. Microbiol. 2002, 43, 763–770.

    Article  CAS  PubMed  Google Scholar 

  87. M. Kern, J. Scheithauer, R. G. Kranz, J. Simon, Microbiology 2010, 156, 3773–3781.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  88. J. M. Stevens, D. A. Mavridou, R. Hamer, P. Kritsiligkou, A. D. Goddard, S. J. Ferguson, FEBS J. 2011, 278, 4170–4178.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  89. J. Simon, L. Hederstedt, FEBS J. 2011, 278, 4179–4188.

    Article  CAS  PubMed  Google Scholar 

  90. S. R. Poock, E. R. Leach, J. W. B. Moir, J. A. Cole, D. J. Richardson, J. Biol. Chem. 2002, 277, 23664–23669.

    Article  CAS  PubMed  Google Scholar 

  91. P. C. Mills, G. Rowley, S. Spiro, J. C. D. Hinton, D. J. Richardson, Microbiology 2008, 154, 1218–1228.

    Article  CAS  PubMed  Google Scholar 

  92. M. Kern, J. Volz, J. Simon, Environ. Microbiol. 2011, 13, 2478–2494.

    Article  CAS  PubMed  Google Scholar 

  93. R. K. Poole, Biochem. Soc. Trans. 2005, 33, 176–180.

    Article  CAS  PubMed  Google Scholar 

  94. T. V. Tikhonova, A. Slutsky, A. N. Antipov, K. M. Boyko, K. M. Polyakov, D. Y. Sorokin, R. A. Zvyagilskaya, V. O. Popov, Biochim. Biophys. Acta 2006, 1764, 715–723.

    Article  CAS  PubMed  Google Scholar 

  95. M. Kern, M.G. Klotz, J. Simon, Mol. Microbiol. 2011, 82,1515–1530.

    Article  CAS  PubMed  Google Scholar 

  96. C. G. Mowat, E. Rothery, C. S. Miles, L. McIver, M. K. Doherty, K. Drewette, P. Taylor, M. D. Walkinshaw, S. K. Chapman, G. A. Reid, Nat. Struct. Mol. Biol. 2004, 11, 1023–1024.

    Article  CAS  PubMed  Google Scholar 

  97. S. J. Atkinson, C. G. Mowat, G. A. Reid, S. K. Chapman, FEBS Lett. 2007, 581, 3805–3808.

    Article  CAS  PubMed  Google Scholar 

  98. K. M. Polyakov, K. M. Boyko, T. V. Tikhonova, A. Slutsky, A. N. Antipov, R. A. Zvyagilskaya, A. N. Popov, G. P Bourenkov, V. S. Lamzin, V. O. Popov, J. Mol. Biol. 2009, 389, 846–862

    Google Scholar 

  99. T. V. Tikhonova, A. A. Trofimov, V. O. Popov, Biochemistry (Moscow) 2012, 77, 1129–1138.

    Article  CAS  Google Scholar 

  100. T. V. Tikhonova, A. Tikhonov, A. Trofimov, K. M. Polyakov, K. M. Boyko, E. Cherkashin, T. Rakitina, D. Y. Sorokin, V. O. Popov, FEBS J. 2012, 279, 4052–4061.

    Article  CAS  PubMed  Google Scholar 

  101. N. Igarashi, H. Moriyama, T. Fujiwara, Y. Fukumori, N. Tanaka, Nat. Struct. Biol. 1997, 4, 276–284.

    Article  CAS  PubMed  Google Scholar 

  102. J. Kostera, M. D. Youngblut, J. M. Slosarczyk, A. A. Pacheco, J. Biol. Inorg. Chem. 2008, 13, 1073–1083

    Article  CAS  PubMed  Google Scholar 

  103. J. Kostera, J. McGarry, A. A. Pacheco, Biochemistry 2010, 49, 8546–8553.

    Article  CAS  PubMed  Google Scholar 

  104. R. Schnell, T. Sandalova, U. Hellman, Y. Lindqvist, G. Schneider, J. Biol. Chem. 2005, 280, 27319–27328.

    Article  CAS  PubMed  Google Scholar 

  105. S. B. Mohan, M. Schmid, M. S. M. Jetten, J. Cole, FEMS Microbiol. Ecol. 2004, 49, 433–443.

    Article  CAS  PubMed  Google Scholar 

  106. J. W. Erisman, A. Bleeker, J. Galloway, M. S. Sutton, Environ. Pollut. 2007, 150, 140–149.

    Article  CAS  PubMed  Google Scholar 

  107. D. Fowler, M. Coyle, U. Skiba, M. A. Sutton, J. N. Cape, S. Reis, L. J. Sheppard, A. Jenkins, B. Grizzetti, J. N. Galloway, P. Vitousek, A. Leach, A. F. Bouwman, K. Butterbach–Bahl, F. Dentener, D. Stevenson, M. Amann, M. Voss, Phil. Trans. R. Soc. B 2013, 368, 20130164; doi: 10.1098/rstb.2013.0164.

  108. M. Voss, H. W. Bange, J. W. Dippner, J. J. Middelburg, J. P. Montoya, B. Ward, Phil. Trans. R. Soc. B 2013, 368, 20130121; doi: 10.1098/rstb.2013.0121.

    Article  PubMed Central  PubMed  Google Scholar 

  109. M. Giles, N. Morley, E. M. Baggs, T. J. Daniell, Front. Microbiol. 2012, 3, article 407, 1–16.

    Google Scholar 

  110. G. Rowley, D. Hensen, H. Felgate, A. Arkenberg, C. Appia-Ayme, K. Prior, C. Harrington, S. Field, J. N. Butt, D. J. Richardson, Biochem. J. 2012, 441, 755–762.

    Article  CAS  PubMed  Google Scholar 

  111. M. A. Streminska, H. Felgate, G. Rowley, D. J. Richardson, E. M. Baggs, Environ. Microbiol. Rep. 2012, 4, 66–71.

    Article  CAS  PubMed  Google Scholar 

  112. M. Luckmann, D. Mania, M. Kern, L. R. Bakken, Å. Frostegård, J. Simon, Microbiology 2014, 160, 1749–1759.

    Google Scholar 

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Acknowledgments

The authors are grateful to Sascha Hein and Melanie Kern (Technische Universität Darmstadt) for providing unpublished data on NrfA phylogeny, and to Oliver Einsle (Albert-Ludwigs-Universität Freiburg) for stimulating discussions. Cited own work was supported by grants from the Deutsche Forschungsgemeinschaft (DFG) (JS, PK) and the Volkswagen-Stiftung (PK).

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  1. Microbial Energy Conversion and Biotechnology, Department of Biology, Technische Universität Darmstadt, Schnittspahnstrasse 10, D-64287, Darmstadt, Germany

    Jörg Simon

  2. Fachbereich Biologie, Universität Konstanz, Universitätsstrasse 10, D-78457, Konstanz, Germany

    Peter M. H. Kroneck

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  1. Univ. Konstanz Fachbereich Biologie, Konstanz, Baden-Württemberg, Germany

    Peter M.H. Kroneck

  2. Facultad de Química Universidad Autónoma de México, Departamento de Química Inorganica y Nuclear, México, Distrito Federal, Mexico

    Martha E. Sosa Torres

Abbreviations

Abbreviations

anammox:

anaerobic ammonium oxidation (= comproportionation of nitrite and ammonium to form dinitrogen)

DFT:

density functional theory

DNA:

deoxyribonucleic acid

EPR:

electron paramagnetic resonance

Fe/S:

iron-sulfur center

Hao:

hydroxylamine oxidoreductase

HOMO:

highest occupied molecular orbital

LUMO:

lowest unoccupied molecular orbital

MCC:

multiheme cytochrome c family

MK:

menaquinone

MKH2 :

menaquinol/menahydroquinone

NapA:

periplasmic nitrate reductase

Nrf:

nitrite reduction by formate

NrfA:

pentaheme cytochrome c nitrite reductase

Onr:

octaheme cytochrome c nitrite reductase

Otr:

octaheme cytochrome c tetrathionate reductase

PCR:

polymerase chain reaction

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© 2014 Springer Science+Business Media Dordrecht

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Simon, J., Kroneck, P.M.H. (2014). The Production of Ammonia by Multiheme Cytochromes c . In: Kroneck, P., Torres, M. (eds) The Metal-Driven Biogeochemistry of Gaseous Compounds in the Environment. Metal Ions in Life Sciences, vol 14. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9269-1_9

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