Advertisement

Hydrogen Sulfide: A Toxic Gas Produced by Dissimilatory Sulfate and Sulfur Reduction and Consumed by Microbial Oxidation

  • Larry L. Barton
  • Marie-Laure Fardeau
  • Guy D. FauqueEmail author
Part of the Metal Ions in Life Sciences book series (MILS, volume 14)

Abstract

Sulfur is an essential element for the synthesis of cysteine, methionine, and other organo-sulfur compounds needed by living organisms. Additionally, some prokaryotes are capable of exploiting oxidation or reduction of inorganic sulfur compounds to energize cellular growth. Several anaerobic genera of Bacteria and Archaea produce hydrogen sulfide (H2S), as a result of using sulfate (SO 4 2 − ), elemental sulfur (S0), thiosulfate (S2O 3 2 − ), and tetrathionate (S4O 6 2 − ) as terminal electron acceptors. Some phototrophic and aerobic sulfur bacteria are capable of using electrons from oxidation of sulfide to support chemolithotrophic growth. For the most part, biosulfur reduction or oxidation requires unique enzymatic activities with metal cofactors participating in electron transfer. This review provides an examination of cytochromes, iron-sulfur proteins, and sirohemes participating in electron movement in diverse groups of sulfate-reducing, sulfur-reducing, and sulfide-oxidizing Bacteria and Archaea.

Keywords

hydrogen sulfide production sulfate reduction sulfide oxidation sulfite reduction sulfur cycle 

Notes

Acknowledgments

Sequence data were produced by the US Department of Energy Joint Genome Institute http://www.jgi.doe.gov/ in collaboration with the user community.

References

  1. 1.
    R. Wang, Physiol. Rev. 2012, 92, 791–896.PubMedGoogle Scholar
  2. 2.
    L. L. Barton, G. D. Fauque, Adv. Appl. Microbiol. 2009, 68, 41–98.PubMedGoogle Scholar
  3. 3.
    R. Rabus, T. A. Hansen, F. Widdel, in The Prokaryotes, Vol. 2, Ecophysiology and Biochemistry, Eds M. Dworkin, S. Falkow, E. Rosenberg, K.-K. Scheifer, E. Stackebrandt, Springer, Berlin, 2006, pp. 659–768.Google Scholar
  4. 4.
    G. D. Fauque, in Biotechnology Handbooks, Vol. 8, Sulfate-Reducing Bacteria, Ed L.L. Barton, Plenum Press, New York, 1995, pp. 217–241.Google Scholar
  5. 5.
    J. Loubinoux, J.-P. Bronowicki, I. A. C. Pereira, J.-L. Mougenel, A. LeFaou, FEMS Microbiol. Ecol. 2002, 40, 107–112.PubMedGoogle Scholar
  6. 6.
    G. Muyzer, A. J. M. Stams, Nature Rev. Microbiol. 2008, 6, 441–454.Google Scholar
  7. 7.
    B. Ollivier, J.-L. Cayol, G. Fauque, in Sulphate-Reducing Bacteria: Environmental and Engineered Systems, Eds L. L. Barton, W. A. Hamilton, Cambridge University Press, Cambridge, UK, 2007, pp. 305–328.Google Scholar
  8. 8.
    Y. A. Shen, R. Buick, D. E. Canfield, Nature 2001, 410, 77–81.PubMedGoogle Scholar
  9. 9.
    Y. Shen, R. Buick, Earth-Sci. Rev. 2004, 64, 243–272.Google Scholar
  10. 10.
    G. Fauque, B. Ollivier, in Microbial Diversity and Bioprospecting, Ed A.T. Bull, ASM Press, Washington, D.C., 2004, pp. 169–176.Google Scholar
  11. 11.
    H. Castro, N. Williams, A. Ogram, FEMS Microbiol. Ecol. 2000, 31, 1–9.PubMedGoogle Scholar
  12. 12.
    V. M. Gumerov, A Mardanov, A Beletsky, M. Prokofeva, E. A. Bonch-Osmolovskaya, N. Ravin, K. Skyrabin, J. Bacteriol. 2011, 193, 2355–2356.Google Scholar
  13. 13.
    L. Jabari, H. Gannoun, J.-L. Cayol, M. Hamdi, B. Ollivier, G. Fauque, M.-L. Fardeau, Int. J. Syst. Evol. Microbiol. 2013, 63, 2082–2087.PubMedGoogle Scholar
  14. 14.
    H. Cypionka, Annu. Rev. Microbiol. 2000, 54, 827–848.PubMedGoogle Scholar
  15. 15.
    G. Fauque, J. LeGall, L. L. Barton, in Variations in Autotrophic Life, Eds J. M. Shively, L. L. Barton, Academic Press, London, 1991, pp. 271–337.Google Scholar
  16. 16.
    J. LeGall, G. Fauque, in Biology of Anaerobic Microorganisms, Ed A. J. B. Zehnder, Wiley, New York, 1988, pp. 587–639.Google Scholar
  17. 17.
    J. J. G. Moura, P. Gonzalez, I. Moura, G. Fauque, in Sulphate-Reducing Bacteria: Environmental and Engineered Systems, Eds L. L. Barton, W. A. Hamilton, Cambridge University Press, Cambridge, UK, 2007, pp. 241–264.Google Scholar
  18. 18.
    H. D. Peck, Jr., Proc. Natl. Acad. Sci. USA 1959, 45, 701–708.PubMedCentralPubMedGoogle Scholar
  19. 19.
    D. R. Kremer, M. Veenhuis, G. Fauque, H. D. Peck, Jr., J. LeGall, J. Lampreia, J. J. Moura, T. A. Hansen, Arch. Microbiol. 1988, 150, 296–301.Google Scholar
  20. 20.
    J. Simon, P. M. H. Kroneck, Adv. Microbial Physiol. 2013, 62, 45–117.Google Scholar
  21. 21.
    G. Fauque, H. D. Peck, Jr., J. J. G. Moura, B. H. Huynh, Y. Berlier, D. V. DerVartanian, M. Teixeira, A. E. Przybila, P. A. Lespinat, I. Moura, J. LeGall, FEMS Microbiol. Rev. 1988, 54, 299–344.Google Scholar
  22. 22.
    J. J. G. Moura, I. Moura, M. Teixeira, A. V. Xavier, G. Fauque, J. LeGall, in Metal Ions in Biological Systems, Vol. 23, Nickel and Its Role in Biology, Ed H. Sigel, Marcel Dekker Inc., New York, 1988, pp. 285–314.Google Scholar
  23. 23.
    I. A. C. Pereira, A. V. Xavier, in Encyclopedia of Inorganic Chemistry, Ed R. B. King, Vol. 5, 2nd edn, Wiley, New York, 2005, pp. 3360–3376.Google Scholar
  24. 24.
    I. A. C. Pereira, in Microbial Sulfur Metabolism, Eds C. Dahl, C. G. Friedrich, Springer, Berlin, 2008, pp. 24–35.Google Scholar
  25. 25.
    G. D. Fauque, L. L. Barton, Adv. Microbial Physiol. 2012, 60, 1–90.Google Scholar
  26. 26.
    G. D. Fauque, Meth. Enzymol. 1994, 243, 353–367.Google Scholar
  27. 27.
    G. Fauque, O. Klimmek, A. Kröger, Meth. Enzymol. 1994, 243, 367–383.Google Scholar
  28. 28.
    A. Kletzin, T. Urich, F. Muller, T. M. Bandeiras, C. M. Gomez, J. Bioenerg. Biomem. 2004, 36, 77–91.Google Scholar
  29. 29.
    A. Kletzin, in Archaea: Evolution, Physiology, and Molecular Biology, Eds R. A. Garrett, H.-P. Klenk, Blackwell Publishing Ltd., Madden, MA, USA, 2007, pp. 261–274.Google Scholar
  30. 30.
    A. LeFaou, B. S. Rajagopal, L. Daniels, G. Fauque, FEMS Microbiol. Rev. 1990, 75, 351–382.Google Scholar
  31. 31.
    J. Boulègue, Phosphorus Sulfur Silicon Relat. Elem. 1978, 5, 127–128.Google Scholar
  32. 32.
    R. Hedderich, O. Klimmek, A. Kröger, R. Dirmeier, M. Keller, K. O. Stetter, FEMS Microbiol. Rev. 1999, 22, 353–381.Google Scholar
  33. 33.
    N. Pfennig, H. Biebl, Arch. Microbiol . 1976, 110, 3–12.Google Scholar
  34. 34.
    F. Widdel, N. Pfennig, in The Prokaryotes, Eds A. Balows, H. G. Trüper, M. Dworkin, W. Harder, K. H. Schleifer, 2nd edn, Vol. 4, New York, Springer, 1992, pp. 3379–3389.Google Scholar
  35. 35.
    A. Zöphel, M. C. Kennedy, H. Beinert, P. M. H. Kroneck, Arch. Microbiol. 1988, 150, 72–77.Google Scholar
  36. 36.
    A. Zöphel, M. C. Kennedy, H. Beinert, P. M. H. Kroneck, Eur. J. Biochem. 1991, 195, 849–856.PubMedGoogle Scholar
  37. 37.
    H. Biebl, N. Pfennig, Arch. Microbiol. 1977, 112, 115–117.PubMedGoogle Scholar
  38. 38.
    O. Ben Dhia Thabet, T. Wafa, K. Eltaief, J.-L. Cayol, M. Hamdi, G. Fauque, M.-L. Fardeau, Curr. Microbiol. 2011, 62, 486–491.Google Scholar
  39. 39.
    B. Ollivier, C. E. Hatchikian, G. Prensier, J. Guezennec, J.-L. Garcia, Int. J. Syst. Bacteriol. 1991, 41, 74–81.Google Scholar
  40. 40.
    R. Schauder, A. Kröger, Arch. Microbiol. 1993, 159, 491–497.Google Scholar
  41. 41.
    R. Thauer, K. Jungermann, K. Decker, Bacteriol. Rev. 1977, 41, 100–180.PubMedCentralPubMedGoogle Scholar
  42. 42.
    P. Schönheit, T. Schäfer, World J. Microbiol. Biotech. 1995, 11, 26–57.Google Scholar
  43. 43.
    K. O. Stetter, G. Gaag, Nature 1983, 305, 309–311.Google Scholar
  44. 44.
    K. Finster, J. Sulf. Chem. 2008, 29, 281–292.Google Scholar
  45. 45.
    F. Bak, N. Pfennig, Arch. Microbiol. 1987, 147, 184–189.Google Scholar
  46. 46.
    K. Finster, W. Liesack, B. Thamdrup, Appl. Environ. Microbiol. 1998, 64, 119–125.PubMedCentralPubMedGoogle Scholar
  47. 47.
    M. Kramer, H. Cypionka, Arch. Microbiol. 1989, 151, 232–237.Google Scholar
  48. 48.
    P. Philippot, M. Van Zuylen, K. Lepot, C. Fhomazzo, J. Farquhar, M. J. Van Kranendonk, Science 2007, 317, 1534–1537.PubMedGoogle Scholar
  49. 49.
    G. Muyzer, J. G. Kuenen, L. A. Robertson, in The Prokaryotes – Prokaryotic Physiology and Biochemistry, Eds E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, F. Thompson, Springer-Verlag, Berlin, Heidelberg, 2013, pp. 555–588.Google Scholar
  50. 50.
    N.-U. Frigaard, C. Dahl, Adv. Microbial Physiol. 2009, 54, 103–200.Google Scholar
  51. 51.
    J. F. Imhoff, in Sulfur Metabolism in Phototrophic Organisms, Eds R. Hell, C. Dahl, D. Knaff, T. Leustek, Springer, The Netherlands, 2008, pp. 269–287.Google Scholar
  52. 52.
    D.Y. Sorokin, H. Banciu, L. A. Robertson, J. G. Kuenen, M. S. Muntyan, G. Muyzer, in The Prokaryotes – Prokaryotic Physiology and Biochemistry, Eds E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, F. Thompson, Springer-Verlag, Berlin, Heidelberg, 2013, pp. 529–554.Google Scholar
  53. 53.
    M. S. Vandiver, S. H. Snyder, J. Mol. Med. 2012, 90, 255–263.PubMedCentralPubMedGoogle Scholar
  54. 54.
    D. Julian, K. L April, S. Patel, J. R. Stein, S.E. Wohlgemuth, J. Experiment. Biol. 2005, 208, 4109–4122.Google Scholar
  55. 55.
    D. W. Kraus, J. E. Doeller, C.S. Powell, J. Experiment. Biol. 1996, 199, 1343–1352.Google Scholar
  56. 56.
    T. Bagarino, Aquat. Toxicol. 1992, 24, 21–62.Google Scholar
  57. 57.
    P. Nicholls, Biochim. Biophys. Acta 1975, 396, 24–35.PubMedGoogle Scholar
  58. 58.
    R. O. Beauchamp, Jr., J. S. Bus, J. A. Popp, C. J. Boreiko, D. A. Andjelkovich, Crit. Rev. Toxicol. 1984, 13, 25–97.PubMedGoogle Scholar
  59. 59.
    F. Widdel, in Biology of Anaerobic Microorganisms, Ed A. J. B. Zehnder, Wiley, New York, 1988, pp. 469–585.Google Scholar
  60. 60.
    S. M. Caffrey, G. Voordouw, Antonie van Leeuwenhoek. 2010, 97, 11–20.Google Scholar
  61. 61.
    J. M. Akagi, L. L. Campbell, J. Bacteriol. 1963, 86, 563–568.PubMedCentralPubMedGoogle Scholar
  62. 62.
    H. Nakazawa, A. Arakaki, S. Narita-Yamada, I. Yashiro, K. Jinno, N. Aoki, A. Tsuruyama, Y. Okamura, S. Tanikawa, N. Fujita, H. Takeyama, Genome Res. 2009, 19, 1801–1808.PubMedCentralPubMedGoogle Scholar
  63. 63.
    B. Suh, J. M. Akagi, J. Bacteriol. 1969, 99, 210–215.PubMedCentralPubMedGoogle Scholar
  64. 64.
    J. P. Lee, H. D. Peck, Jr., Biochem. Biophys. Res. Commun. 1971, 45, 583–589.PubMedGoogle Scholar
  65. 65.
    J. M. Akagi, V. Adams, J. Bacteriol. 1973, 116, 392–396.PubMedCentralPubMedGoogle Scholar
  66. 66.
    K. Kobayashi, S. Tachibana, M. Ishimoto, J. Biochem. 1969, 65, 155–157.PubMedGoogle Scholar
  67. 67.
    J.-P. Lee, J. LeGall, H. D. Peck, Jr., J. Bacteriol. 1973, 115, 529–542.PubMedCentralPubMedGoogle Scholar
  68. 68.
    R. H. Haschke, L. L. Campbell, J. Bacteriol. 1971, 106, 603–607.PubMedCentralPubMedGoogle Scholar
  69. 69.
    E. C. Hatchikian, J. G. Zeikus, J. Bacteriol. 1983, 153, 2111–1220.Google Scholar
  70. 70.
    W. Nakatsukasa, J. M. Akagi, J. Bacteriol. 1969, 98, 429–433.PubMedCentralPubMedGoogle Scholar
  71. 71.
    E. C. Hatchikian, Arch. Microbiol. 1975, 105, 249–256.PubMedGoogle Scholar
  72. 72.
    R. M. Fitz, H. Cypionka, Arch. Microbiol. 1990, 154, 400–406.Google Scholar
  73. 73.
    M. Broco, M. Rousset, S. Oliveira, C. Rodrigues-Pousada, FEBS Lett. 2005, 579, 4803–4807.PubMedGoogle Scholar
  74. 74.
    H.D. Peck, Jr, J. LeGall, Phil. Trans. R. Soc. B. 1982, 298, 443–466.Google Scholar
  75. 75.
    K. Parey, U. Demmer, E. Warkentin, A. Wynen, U. Ermler, C. Dahl, PLoS ONE 2013, 8: available on line, e74707. doi:10.1371/.Google Scholar
  76. 76.
    N. Sekulic, K. Dietrich, I. Paamann, S. Ort, M. Konrad, A. Lavie, J. Mol. Biol. 2007, 367, 488–500.PubMedCentralPubMedGoogle Scholar
  77. 77.
    C. Dahl, H-G. Koch, O. Keuken, H. G. Trüper, FEMS Microbiol. Lett. 1990, 67, 27–32.Google Scholar
  78. 78.
    O. Y. Gavel, S. A. Bursakov, J. J. Calvete, G. N. George, J. J. Moura, I. Moura, Biochemistry 1998, 37, 16225–16232.PubMedGoogle Scholar
  79. 79.
    Y. Taguchi, M. Sugishima, K. Fukuyama, Biochemistry 2004, 43, 4111–4118.PubMedGoogle Scholar
  80. 80.
    O. Y. Gavel, A. V. Kladova, S. A. Bursakov, J. M. Dias, S. Texeira, V. L. Shnyrov, J. J. G. Moura, I. Moura, M. J. Romão, J. J. Trincão, Acta Crystallogr. Sect. F, Struct. Biol. Cryst. Commun. 2008, 64, 593–595.Google Scholar
  81. 81.
    Y.-L. Chiang, Y.-C. Hsieh, J-Y. Fang, E.-H. Liu, Y.-C. Huang, P. Chuankhayan, J. Jeyakanthan, M.-Y. Liu, S. I. Chan, C.-J. Chen, J. Bacteriol. 2009, 191, 7597–7608.Google Scholar
  82. 82.
    G. Fritz, T. Büchert, P. M. H. Kroneck, J. Biol. Chem. 2002, 277, 26066–26073.PubMedGoogle Scholar
  83. 83.
    B. Meyer, J. Kuever, PLoSONE 2008 3, available online, e1514.doi10.1371/journal.pone.0001514.Google Scholar
  84. 84.
    J. Lampreia, I. Moura, M. Teixeira, H. D. Peck, Jr., J. LeGall, B. H. Huynh, J. J. G. Moura, Eur. J. Biochem. 1990, 188, 653–664.PubMedGoogle Scholar
  85. 85.
    A. R. Ramos, K. L. Keller, J. D. Wall, Front. Microbiol. 2012, 3, 137, available online, doi: 10.3389/fmicb.2012.00137.
  86. 86.
    G. M. Zane, H-c. B. Yen, J. D. Wall, Appl. Environ. Microbiol. 2010, 76, 5500–5509.Google Scholar
  87. 87.
    I. Moura, A. R. Lino, Meth. Enzymol. 1994, 243, 296–303.Google Scholar
  88. 88.
    M. J. Murphy, L. M. Siegel, J. Biol. Chem. 1973, 248, 6911–6919.PubMedGoogle Scholar
  89. 89.
    A. Schiffer, K. Parey, E. Warkentin, K. Diederichs, H. Huber, K. O. Stetter, P. M. Kroneck, U. Ermler, J. Mol. Biol. 2008, 379, 1063–1074.PubMedGoogle Scholar
  90. 90.
    J. Steuber, P. M. H. Kroneck, Inorg. Chim. Acta 1998, 276, 52–57.Google Scholar
  91. 91.
    G. Fritz, A. Schiffer, A. Behrens, T. Buchert, U. Ermler, P. M. H. Kroneck, in Microbial Sulfur Metabolism, Eds C. Dahl, C. G. Friedrich, Berlin, Springer-Verlag, 2008, pp. 13–23.Google Scholar
  92. 92.
    Y.-C. Hsieh, M.-L. Liu, V. C.-C. Wang, Y.-L. Chiang, E.-H. Liu, W. G. Wu, S. I. Shan, C.-J. Chen, Mol. Microbiol. 2010, 78, 1101–1116.PubMedGoogle Scholar
  93. 93.
    T. F. Oliveira, E. Franklin, J. P. Afonso, A. R. Khan, N. J. Oldham, I. A. C. Pereira, M. Archer, Front. Microbiol. 2011, 2, 71 doi:10.3389.Google Scholar
  94. 94.
    F. Grein, I. A. C. Pereira, C. Dahl. J. Bacteriol. 2010, 192, 6369–6377.Google Scholar
  95. 95.
    T. F. Oliveira, C. Vornhein, P. M. Matias, S. S. Venceslau, I. A. C. Pereira, M. Archer, J. Struct. Biol. 2008, 164, 236–239.PubMedGoogle Scholar
  96. 96.
    T. F. Oliveira, C. Vonrhein, P. M. Matias, S. S. Venceslau, I. A. C. Pereira, M. Archer, J. Biol. Chem. 2008, 283, 34141–34149.PubMedCentralPubMedGoogle Scholar
  97. 97.
    R. R. Karkhoff-Schweizer, M. Bruschi, G. Voordouw, Eur. J. Biochem. 1993, 211, 501–507.PubMedGoogle Scholar
  98. 98.
    J. Ostrowski, J.-Y. Wu, D. C. Rueger, B. E. Miller, L. M. Siegel, N. M. Kredich, J. Biol. Chem. 1989, 264, 15726–15737.PubMedGoogle Scholar
  99. 99.
    E. T. Adman, L. Sieker, L. Jensen, J. Biol. Chem. 1976, 248, 3987–3996.Google Scholar
  100. 100.
    M. Bruschi, F. Guerlesquin, FEMS Microbiol. Rev. 1988, 54, 155–176.Google Scholar
  101. 101.
    D. H. George, L. T. Hunt, L. S. L. Yeh, W. C. Barker, J. Mol. Evol. 1985, 22, 117–143.Google Scholar
  102. 102.
    I. Moura, J. LeGall, A. R. Lino, H. D. Peck, Jr., G. Fauque, A. V. Xavier, D. V. DerVartanian, J. J. G. Moura, B. H. Huynh, J. Am. Chem. Soc. 1988, 110, 1075–1082.Google Scholar
  103. 103.
    J. Steuber, H. Cypionka, P. M. H. Kroneck, Arch. Microbiol. 1994, 162, 255–260.Google Scholar
  104. 104.
    J. Steuber, A. F. Arendsen, W. R. Hagen, P. M. H. Kroneck, Eur. J. Biochem. 1995, 233, 873–879.PubMedGoogle Scholar
  105. 105.
    B. M. Wolfe, S. Lui, J. A. Cowan, Eur. J. Biochem. 1994, 223, 79–89.PubMedGoogle Scholar
  106. 106.
    A. J. Pierik, M. G. Duyvis, J. M. L. M. van Helvoort, R. B. J. Wolbert, W. R. Hagen, Eur. J. Biochem. 1992, 205, 111–115.PubMedGoogle Scholar
  107. 107.
    R. H. Pires, S. S. Venceslao, F. Morais, M. Teixeira, A. V. Xavier, I. A. Pereira, Biochemistry 2006, 45, 249–262.PubMedGoogle Scholar
  108. 108.
    R. R. Karkhoff-Schweizer, D. P. W. Huber, G. Voordouw, Appl. Env. Microbiol. 1995, 61, 290–296.Google Scholar
  109. 109.
    N. Mizuno, G. Voordouw, K. Miki, A. Sarai, Y. Higuchi, Structure, 2003, 11, 1133–1140.PubMedGoogle Scholar
  110. 110.
    J. C. Mathews, R. Timkovich, M.-Y. Lin, J. LeGall, Biochemistry 1995, 34, 5248–5251.Google Scholar
  111. 111.
    P. A. Trudinger, J. Bacteriol. 1970, 104, 158–170.PubMedCentralPubMedGoogle Scholar
  112. 112.
    Ø. Larsen, T. Lien, N. K. Birkeland, Extremophiles, 1999, 3, 63–70.PubMedGoogle Scholar
  113. 113.
    D. V. DerVartanian, Meth. Enzymol. 1994, 243, 270–276.PubMedGoogle Scholar
  114. 114.
    N. Klouche, O. Basso, J.-F. Lascourrèges, J.-L. Cayol, P. Thomas, G. Fauque, M.-L. Fardeau, M. Magot, Int. J. Syst. Evol. Microbiol. 2009, 59, 3100–3104.Google Scholar
  115. 115.
    Ø. Larsen, T. Lien, N. K. Birkeland, FEMS Microbiol. Lett. 2000, 186, 41–46.PubMedGoogle Scholar
  116. 116.
    B. R. Crane, L. M. Siegel, E. D. Getzoff, Science, 1995, 270, 59–67.PubMedGoogle Scholar
  117. 117.
    C. Dahl, N. M. Kredich, R. Deutzmann, H. G. Trüper, J. Gen. Microbiol. 1993, 139, 1817–1828.PubMedGoogle Scholar
  118. 118.
    L. Debussche, D. Thibaut, B. Cameron, J. Crouzet, F. Blanche, J. Bacteriol. 1990, 172, 6239–6244.PubMedCentralPubMedGoogle Scholar
  119. 119.
    G. Fauque, A. Lino, M. Czechowski, L. Kang, D. V. DerVartanian, J. J. G. Moura, J. LeGall, I. Moura, Biochim. Biophys. Acta 1990, 1040, 112–118.PubMedGoogle Scholar
  120. 120.
    E. C. Hatchikian, Meth. Enzymol. 1994, 243, 276–295.PubMedGoogle Scholar
  121. 121.
    O. Haouari, M.-L. Fardeau, J.-L. Cayol, G. Fauque, C. Casiot, F. Elbaz-Poulichet, M. Hamdi, B. Ollivier, Syst. Appl. Microbiol. 2008, 31, 38–42.PubMedGoogle Scholar
  122. 122.
    A. M. Stolzenberg, S. H. Strauss, R. H. Holm, J. Am. Chem. Soc. 1981, 103, 4763–4778.Google Scholar
  123. 123.
    C. Dahl, H. G. Trüper, Meth. Enzymol. 2001, 331, 427–441.PubMedGoogle Scholar
  124. 124.
    B. B. Jørgensen, Science, 1990, 249, 152–154.PubMedGoogle Scholar
  125. 125.
    L. Stoffels, M. Krehenbrink, B. C. Berks, G. Unden, J. Bacteriol. 2012, 194, 475–485.PubMedCentralPubMedGoogle Scholar
  126. 126.
    R. Starkey, Soil Sci. 1950, 70, 55–66.Google Scholar
  127. 127.
    S. E. Winter, P. Thiennimitr, M. G. Winter, B. P. Butler, D. L. Huseby, R. W. Crawford, J. M. Russell, C. L. Bevins, L. G. Adams, R. M. Tsolis, J. R. Roth, A. J. Bäumler, Nature 2010, 467, 426–429.PubMedCentralPubMedGoogle Scholar
  128. 128.
    E. F. Johnson, B. Mukhopadhyay, J. Biol. Chem. 2005, 280, 38776–38786.PubMedGoogle Scholar
  129. 129.
    E. F. Johnson, B. Mukhopadhyay, Appl. Env. Microbiol. 2008, 74, 3591–3595.Google Scholar
  130. 130.
    H. Laue, M. Friedrich, J. Ruff, A. M. Cook, J. Bacteriol. 2001, 183, 1727–11733.PubMedCentralPubMedGoogle Scholar
  131. 131.
    G. Harrison, C. Curle, E. J. Laishley, Arch. Microbiol. 1984, 138, 72–78.PubMedGoogle Scholar
  132. 132.
    V. L. Barbosa-Jefferson, F. J. Zhao, S. P. McGrath, N. Morgan, Soil Biol. Biochem. 1998, 30, 553–559.Google Scholar
  133. 133.
    E. L. Barrett, M. A. Clark, Microbiol. Rev. 1987, 51, 195–205.Google Scholar
  134. 134.
    M. Hinojosa-Leon, M. Dubourdieu, J. A. Sanchez-Crispin, M. Chippaux, Biochem. Biophys. Res. Commun. 1986, 136, 577–581.PubMedGoogle Scholar
  135. 135.
    J. L. Burns and T. J. DiChristina, Appl. Environ. Microbiol. 2009, 75, 5209–5217.PubMedCentralPubMedGoogle Scholar
  136. 136.
    A. P. Hinsley, B. C. Berks, Microbiology 2002, 148, 3631–3638.PubMedGoogle Scholar
  137. 137.
    P. Hallenbeck, M. A. Clark, E. L. Barrett, J. Bacteriol. 1989, 171, 3008–3015.PubMedCentralPubMedGoogle Scholar
  138. 138.
    C. J. Huang, E. L. Barrett, J. Bacteriol. 1991, 173, 1544–1553.PubMedCentralPubMedGoogle Scholar
  139. 139.
    L. M. Siegel, P.S. Davis, J. Biol. Chem. 1974, 249, 1587–1598.PubMedGoogle Scholar
  140. 140.
    M. Kern, M. G. Klotz, J. Simon, Mol. Microbiol. 2011, 82, 1515–1530.PubMedGoogle Scholar
  141. 141.
    S. Shirodkar, S. Reed, M. Romine, D. Saffarini, Environ. Microbiol. 2011, 158, 287–293.Google Scholar
  142. 142.
    H. L. Drake, J. M. Akagi, Biochem. Biophys. Res. Commun. 1976, 71, 1214–1219.PubMedGoogle Scholar
  143. 143.
    B. H. Huynh, L. Kang, D. V. DerVartanian, H. D. Peck, Jr., J. LeGall, J. Biol. Chem. 1984, 259, 15373–15376.PubMedGoogle Scholar
  144. 144.
    I. Moura, A. R. Lino, J. J. G. Moura, A. V. Xavier, G. Fauque, H. D. Peck, Jr., J. LeGall, Biochem. Biophys. Res. Commun. 1986, 141, 1032–1041.PubMedGoogle Scholar
  145. 145.
    J. J. G. Moura, I. Moura, H. Santos, A. V. Xavier, M. Scandellari, J. LeGall, Biochem. Biophys. Res. Commun. 1982, 108, 1002–1009.PubMedGoogle Scholar
  146. 146.
    G. Fauque, Doctorat d’Etat Thesis in Physical Sciences, University of Technology of Compiègne, France, 1985, 222 pages.Google Scholar
  147. 147.
    G. Fauque, D. Hervé, J. LeGall, Arch. Microbiol. 1979, 121, 261–264.PubMedGoogle Scholar
  148. 148.
    R. Cammack, G. Fauque, J. J. G. Moura, J. LeGall, Biochim. Biophys. Acta 1984, 784, 68–74.Google Scholar
  149. 149.
    G. D. Fauque, L. L. Barton, J. LeGall, Sulphur in Biology: Ciba Foundation Symposium 1980, 72, 71–86.Google Scholar
  150. 150.
    A. S. Alves, C. M. Paquete, B. M. Fonseca, R. O. Louro, Metallomics 2011, 3, 349–353.PubMedGoogle Scholar
  151. 151.
    I. A. C. Pereira, I. Pacheco, M.-Y. Liu, J. LeGall, A. V. Xavier, M. Teixeira, Eur. J. Biochem. 1997, 248, 323–328.PubMedGoogle Scholar
  152. 152.
    S. Laska, F. Lottspeich, A. Kletzin, Microbiology 2003, 149, 2357–2371.PubMedGoogle Scholar
  153. 153.
    M. Keller, R. Dirmeier, Meth. Enzymol. 2001, 331, 442–451.PubMedGoogle Scholar
  154. 154.
    S. L. Bridger, S. M. Clarkson, K. Stirrett, M. B. Debarry, G. L. Lipscomb, G. J. Schut, J. Westpheling, R. A. Scott, M. W. W. Adams, J. Bacteriol. 2011, 193, 6498–6504.PubMedCentralPubMedGoogle Scholar
  155. 155.
    A. Kletzin, in Microbial Sulfur Metabolism, Eds C. Dahl, C. G. Friedrich, Springer, Berlin, 2008, pp. 184–201.Google Scholar
  156. 156.
    T. Urich, C. M. Gomes, A. Kletzin, C. Frazao, Science 2006, 311, 996–1000.PubMedGoogle Scholar
  157. 157.
    W. Purschke, C. L. Schmidt, A. Petersen, G. Schafer, J. Bacteriol. 1997, 179, 1344–1353.PubMedCentralPubMedGoogle Scholar
  158. 158.
    J. A. Brito, F. L. Sousa, M. Stelter, T. M. Bandeiras, C. Vonrhein, M. Teixeira, M. M. Pereira, M. Archer, Biochemistry 2009, 48, 5613–5622.PubMedGoogle Scholar
  159. 159.
    M. Schedel, M. Vanselow, H. G. Trüper, Arch. Microbiol. 1979, 121, 29–36Google Scholar
  160. 160.
    F. Grimm, B. Franz, C. Dahl, in Microbial Sulfur Metabolism, Eds C. Dahl, C. G. Friedrich, Springer, Berlin, 2008, pp. 101–116.Google Scholar
  161. 161.
    R. Hille, Chem. Rev. 1996, 96, 2757–2816PubMedGoogle Scholar
  162. 162.
    U. Kappler, M. J. Maher, Cell. Mol. Life Sci. 2013, 70, 977–992.Google Scholar
  163. 163.
    H. Sakurai, T. Ogawa, M. Shiga, K. Inoue, Photosynth. Res. 2010, 104, 163–176.PubMedGoogle Scholar
  164. 164.
    L. H. Gregersen, D. A Bryant, N.-U. Frigaard, Front. Microbiol. 2011, available online, doi:  10.3389/fmicb.2011.00116.
  165. 165.
    J. P. Lee, C. Yi, J. LeGall, H. Peck, Jr, J. Bacteriol. 1973, 115, 453–455.PubMedCentralPubMedGoogle Scholar
  166. 166.
    A. F. Arendsen, M. F. Verhagen, R. B. Wolbert, A. J. Pierik, A. J. Stams, M. S. Jetten, W. R. Hagen, Biochemistry 1993, 32, 10323–10330.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Larry L. Barton
    • 1
  • Marie-Laure Fardeau
    • 2
  • Guy D. Fauque
    • 2
    Email author
  1. 1.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  2. 2.Institut Méditerranéen d’Océanologie (MIO)Aix-Marseille Université, USTV, UMR CNRS 7294/IRD 235Marseille Cedex 09France

Personalised recommendations