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Recent progress in hydrogenase and its biotechnological application for viable hydrogen technology

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Abstract

Despite increasing interest in hydrogen (H2) as an alternative energy carrier, the current production of H2 still depends on fossil fuels. Biotechnological hydrogen production can provide a more sustainable way to generate H2. Hydrogenases are key enzymes involved in hydrogen metabolism of microorganisms with roles of H2 oxidation or evolution. They have potential applications in H2 production in vivo, in vitro and fuel cell. Important achievements have been made over the past decade in our understanding of hydrogenase and its biotechnological application as catalyst for H2 production and fuel cell. This review summarizes recent progress in the study of hydrogenases, involving strategies for biosynthesis, maturation process, isolation of novel hydrogenases, heterologous expression system, structural feature of oxygen (O2)-tolerant hydrogenases, and biotechnological applications for viable H2 technology.

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References

  1. J.M. Walter, D. Greenfield and J. Liphardt, Curr. Opin. Biotechnol., 21, 265 (2010).

    Article  CAS  Google Scholar 

  2. J. S. Dukes, Climatic Change, 61, 31 (2003).

    Article  CAS  Google Scholar 

  3. B. Friedrich, J. Fritsch and O. Lenz, Curr. Opin. Biotechnol., 22 358 (2011).

    Article  CAS  Google Scholar 

  4. M. Balat, Int. J. Hydrog. Energy, 33, 4013 (2008).

    Article  CAS  Google Scholar 

  5. D. Das and T. N. Veziroglu, Int. J. Hydrog. Energy, 33, 6046 (2008).

    Article  CAS  Google Scholar 

  6. J. H. Park, D. Lee, H. C. Lee and E. D. Park, Korean J. Chem. Eng., 27, 1132 (2010).

    Article  CAS  Google Scholar 

  7. D. B. Levin, L. Pitt and M. Love, Int. J. Hydrog. Energy, 29, 173 (2004).

    Article  CAS  Google Scholar 

  8. R.G. Sawers, S. P. Balantine and D. H. Boxer, J. Bacteriol., 164, 1324 (1985).

    CAS  Google Scholar 

  9. P.M. Vignais, B. Billoud and J. Meyer, FEMS Microbiol. Rev., 25, 455 (2001).

    CAS  Google Scholar 

  10. T.V. Laurinavichene, N. A. Zorin and A. A. Tsygankov, Arch. Microbiol., 178, 437 (2002).

    Article  CAS  Google Scholar 

  11. K. Rabaey and W. Verstraete, Trends Biotechnol., 23, 291 (2005).

    Article  CAS  Google Scholar 

  12. P. M. Vignais and B. Billoud, Chem. Rev., 107, 4206 (2007).

    Article  CAS  Google Scholar 

  13. M. Stephen and L. H. Stickland, Biochem. J., 25, 205 (1931).

    Google Scholar 

  14. M. Frey, Chembiochem, 3, 153 (2002).

    Article  CAS  Google Scholar 

  15. M.W. Adams and D. Hall, Biochem. J., 183, 11 (1979).

    CAS  Google Scholar 

  16. H. Nishihara, Y. Miyashita, K. Aoyama, T. Kodama, Y. Igarashi and Y. Takamura, Biochem. Biophy. Res. Comm., 232, 766 (1997).

    Article  CAS  Google Scholar 

  17. T. Buhrke, O. Lenz, N. Krauss and B. Friedrich, J. Biol. Chem., 280, 23791 (2005).

    Article  CAS  Google Scholar 

  18. M. Winkler, S. Kawelke and T. Happe, Bioresour. Technol., 102, 8493 (2011).

    Article  CAS  Google Scholar 

  19. H. Gaffron and J. Rubin, J. Gen. Physiol., 26, 219 (1942).

    Article  CAS  Google Scholar 

  20. V. C. Kalia, S. Lal, R. Ghai, M. Mandal and A. Chauhan, Trends Biotechnol., 21, 152 (2003).

    Article  CAS  Google Scholar 

  21. A. Volbeda, M. H. Charon, C. Piras, E. C. Hatchikian, M. Frey and J. C. Fontecilla-Camps, Nature, 373, 580 (1995).

    Article  CAS  Google Scholar 

  22. Y. Montet, P. Amara, A. Volbeda, X. Vernede, E. C. Hatchikian, M. J. Field, M. Frey and J. C. Fontecilla-Camps, Nat. Struct. Biol., 4, 523 (1997).

    Article  CAS  Google Scholar 

  23. L. Casalot and M. Rousset, Trends Microbiol., 9, 228 (2001).

    Article  CAS  Google Scholar 

  24. O. Lenz, A. Gleiche, A. Strack and B. Friedrich, J. Bacteriol., 187, 6590 (2005).

    Article  CAS  Google Scholar 

  25. E. Theodoratou, A. Paschos, Mintz-Weber and A. Böck, Arch. Microbiol., 173, 110 (2000).

    Article  CAS  Google Scholar 

  26. L. Forzi and R. G. Sawers, Biometals, 20, 565 (2007).

    Article  CAS  Google Scholar 

  27. M. Blokesch, A. Paschos, E. Theodoratou, A. Bauer, M. Hube, S. Huth and A. Böck, Biochem. Soc. Trans., 30, 674 (2002).

    Article  CAS  Google Scholar 

  28. T. Maier and A. Böck, Biochemistry, 35, 10089 (1996).

    Article  CAS  Google Scholar 

  29. R. Rossmann, M. Sauter, F. Lottspeich and A. Böck, Eur. J. Biochem., 220, 377 (1994).

    Article  CAS  Google Scholar 

  30. L. F. Wu, A. Chanal and A. Rodrigue, Arch. Microbiol., 173, 319 (2000).

    Article  CAS  Google Scholar 

  31. N. Blaudeck, G. A. Sprenger, R. Freudl and T. Wiegert, J. Bacteriol., 183, 604 (2001).

    Article  CAS  Google Scholar 

  32. J.Y. H. Kim, B.H. Jo and H. J. Cha, J. Biotechnol., 155, 312 (2011).

    Article  CAS  Google Scholar 

  33. A. Dubini and F. Sargent, FEBS Lett., 549, 141 (2003).

    Article  CAS  Google Scholar 

  34. M.W. Adams, Biochim. Biophys. Acta, 1020, 115 (1990).

    Article  CAS  Google Scholar 

  35. T. Happe and J. D. Naber, Eur. J. Biochem., 214, 475 (1993).

    Article  CAS  Google Scholar 

  36. F.G. Voncken, B. Boxma, A.H. van Hoek, A. S. Akhmanova, G. D. Vogels, M. Huynen, M. Veenhuis and J. H. Hackstein, Gene, 284, 103 (2002).

    Article  CAS  Google Scholar 

  37. Y. Nicolet, A. L. de Lacey, X. Vernede, V.M. Fernandez, E. C. Hatchikian and J. C. Fontecilla-Camps, J. Am. Chem. Soc., 123, 1596 (2001).

    Article  CAS  Google Scholar 

  38. S. Stripp, O. Sanganas, T. Happe and M. Haumann, Biochemistry, 48, 5042 (2009).

    Article  CAS  Google Scholar 

  39. L. Florin, A. Tsokoglou and T. Happe, J. Biol. Chem., 276, 6125 (2001).

    Article  CAS  Google Scholar 

  40. M. Winkler, B. Heil, B. Heil and T. Happe, Biochim. Biophys. Acta, 1576, 330 (2002).

    Article  CAS  Google Scholar 

  41. A. J. Pierik, M. Hulstein, W. R. Hagen and S. P. J. Albracht, Eur. J. Biochem., 258, 572 (1998).

    Article  CAS  Google Scholar 

  42. H. J. Fan and M. B. Hall, J. Am. Chem. Soc., 123, 3828 (2001).

    Article  CAS  Google Scholar 

  43. Y. Nicolet, C. Cavazza and J. C. Fontecilla-Camps, J. Inorg. Biochem., 91, 1 (2002).

    Article  CAS  Google Scholar 

  44. W. Lubitz, E. Reijerse and M. van Gastel, Chem. Rev., 107, 4331 (2007).

    Article  CAS  Google Scholar 

  45. Y. Nicolet, C. Piras, P. Legrand, C. E. Hatchikian and J. C. Fontecilla-Camps, Structure, 7, 13 (1999).

    Article  CAS  Google Scholar 

  46. M.C. Posewitz, P.W. King, S. L. Smolinski, L. Zhang, M. Seibert and M. L. Ghirardi, J. Biol. Chem., 279, 25711 (2004).

    Article  CAS  Google Scholar 

  47. D.W. Mulder, E. S. Boyd, R. Sarma, R. K. Lange, J. A. Endrizzi, J. B. Broderick and J.W. Peters, Nature, 465, 248 (2010).

    Article  CAS  Google Scholar 

  48. F. J. Hanus, R. J. Maier and H. J. Evans, Proc. Natl. Acad. Sci. USA, 76, 1788 (1979).

    Article  CAS  Google Scholar 

  49. R. J. Maier, N. E. R. Campbell, F. J. Hanus, F. B. Simpson, S. A. Russell and H. J. Evans, Proc. Natl. Acad. Sci. USA, 75, 3258 (1978).

    Article  CAS  Google Scholar 

  50. S. T. Lim, Plant Physiol., 62, 609 (1978).

    Article  CAS  Google Scholar 

  51. E. Feigenblum and A. I. Krasna, Biochim. Biophys. Acta, 141, 250 (1967).

    Article  CAS  Google Scholar 

  52. J. Mishra, S. Khurana, N. Kumar, A. K. Ghosh and D. Das, Biochem. Biophy. Res. Comm., 324, 679 (2004).

    Article  CAS  Google Scholar 

  53. M. Calusinska, B. Joris and A. Wilmotte, Lett. Appl. Microbiol., 53, 473 (2011).

    Article  CAS  Google Scholar 

  54. J.Y. H. Kim, H. J. Jung and H. J. Cha, Enzyme Microb. Technol., 42, 1 (2007).

    Article  CAS  Google Scholar 

  55. R. A. Haugland, F. J. Hanus, M. A. Cantrell and H. J. Evans, Appl. Environ. Microbiol., 45, 892 (1983).

    CAS  Google Scholar 

  56. C. T. Gray and H. Gest, Science, 148, 186 (1965).

    Article  CAS  Google Scholar 

  57. A. S. Bingham, P. R. Smith and J.R. Swartz, Int. J. Hydrog. Energy, 37, 2965 (2012).

    Article  CAS  Google Scholar 

  58. M. L. Ghirardi, L. Zhang, J.W. Lee, T. Flynn, M. Seibert, E. Greenbaum and A. Melis, Trends Biotechnol., 18, 506 (2000).

    Article  CAS  Google Scholar 

  59. G. Maróti, Y. Tong, S. Yooseph, H. Baden-Tillson, H.O. Smith and K. L. Kovács, Appl. Environ. Microbiol., 75, 5821 (2009).

    Article  CAS  Google Scholar 

  60. P. M. Vignais, Results Probl. Cell Differ., 45, 223 (2008).

    Article  CAS  Google Scholar 

  61. C.M. English, C. Eckert, K. Brown, M. Seibert and P.W. King, Dalton Trans., 45, 9970 (2009).

    Article  Google Scholar 

  62. K. Sybirna, T. Antoine, P. Lindberg, V. Fourmond, M. Rousset, V. Mejean and H. Bottin, BMC Biotechnol., 8, 73 (2008).

    Article  CAS  Google Scholar 

  63. Y. Asada, Y. Koike, J. Schnackenberg, M. Miyake, I. Uemura and J. Miyake, Biochim. Biophys. Acta, 1490, 269 (2000).

    Article  CAS  Google Scholar 

  64. P. Berto, S. D’Adamo, E. Bergantino, F. Vallese, G.M. Giacometti and P. Costantini, Biochem. Biophys. Res. Comm., 405, 678 (2011).

    Article  CAS  Google Scholar 

  65. G. Voordouw, W. R. Hagen, K.M. Kruse-Wolters, A. van Berkel-Arts and C. Veeger, Eur. J. Biochem., 162, 31 (1987).

    Article  CAS  Google Scholar 

  66. M. F. Gorwa, C. Croux and P. Soucaille, J. Bacteriol., 178, 2668 (1996).

    CAS  Google Scholar 

  67. M. Atta and J. Meyer, Biochim. Biophys. Acta, 1476, 368 (2000).

    Article  CAS  Google Scholar 

  68. P.W. King, M. C. Posewitz, M. L. Ghirardi and M. Seibert, J. Bacteriol., 188, 2163 (2006).

    Article  CAS  Google Scholar 

  69. L. Girbal, G. von Abendroth, M. Winkler, P. M. C. Benton, I. Meynial-Salles, C. Croux, J.W. Peters, T. Happe and P. Soucaille, Appl. Environ. Microbiol., 71, 2777 (2005).

    Article  CAS  Google Scholar 

  70. G. M. Mura, P. Pedroni, C. Pratesi, G. Galli, L. Serbolisca and G. Grandi, Microbiology, 142, 829 (1996).

    Article  CAS  Google Scholar 

  71. C. Grzeszik, M. Lubbers, M. Reh and H.G. Schlegel, Microbiology, 143, 1271 (1997).

    Article  CAS  Google Scholar 

  72. M. Rousset, V. Magro, N. Forget, B. Guigliarelli, J. Belaich and E.C. Hatchikian, J. Bacteriol., 180, 4982 (1998).

    CAS  Google Scholar 

  73. A. Porthun, M. Bernhard and B. Friedrich, Arch. Microbiol., 177, 159 (2002).

    Article  CAS  Google Scholar 

  74. A. Yoshida, T. Nishimura, H. Kawaguchi, M. Inui and H. Yukawa, Appl. Microbiol. Biotechnol., 74, 754 (2007).

    Article  CAS  Google Scholar 

  75. I. Akkerman, M. Janssen, J. Rochac and R. H. Wijlels, Int. J. Hydrog. Energy, 27, 1195 (2002).

    Article  CAS  Google Scholar 

  76. P. C. Hallenbeck and J. R. Benemann, Int. J. Hydrog. Energy, 27, 1185 (2002).

    Article  CAS  Google Scholar 

  77. K. A. Vincent, J. A. Cracknell, O. Lenz, I. Zebger, B. Friedrich and F. A. Armstrong, Proc. Natl. Acad. Sci. USA, 102, 16951 (2005).

    Article  CAS  Google Scholar 

  78. A. F. Wait, A. Parkin, G.M. Morley, L. dos Santos and Fraser A. Armstrong, J. Phys. Chem. C, 114, 12003 (2010).

    Article  CAS  Google Scholar 

  79. Y. Shomura, K. S. Yoon, H. Nishihara and Y. Higuchi, Nature, 479, 253 (2011).

    Article  CAS  Google Scholar 

  80. J. Fritsch, P. Scheerer, S. Frielingsdorf, S. Kroschinsky, B. Friedrich, O. Lenz and C.M. Spahn, Nature, 479, 249 (2011).

    Article  CAS  Google Scholar 

  81. E. Lojou, Electrochim. Acta, 56, 10385 (2011).

    Article  CAS  Google Scholar 

  82. M. Pandelia, W. Lubitz and W. Nitschke, Biochim. Biophys. Acta, 1817, 1565 (2012).

    Article  CAS  Google Scholar 

  83. G. Y. Jung, J. R. Kim, J. Y. Park and S. H. Park, Int. J. Hydrog. Energy, 27, 601 (2002).

    Article  CAS  Google Scholar 

  84. A. Melis, L. Zhang, M. Forestier, M. L. Ghirardi and M. Seibert, Plant Physiol., 122, 127 (2000).

    Article  CAS  Google Scholar 

  85. A. Melis, Int. J. Hydrog. Energy, 27, 1217 (2002).

    Article  CAS  Google Scholar 

  86. B. Esper, A. Badura and M. Rögner, Trends Plant Sci., 11, 543 (2006).

    Article  CAS  Google Scholar 

  87. R. Surzycki, L. Cournac, G. Peltier and J.D. Rochaix, Proc. Natl. Acad. Sci. USA, 104, 17548 (2007).

    Article  CAS  Google Scholar 

  88. M.G. Esquível, H. M. Amaro, T. S. Pinto, P. S. Fevereiro and F.X. Malcata, Trends Biotechnol., 29, 595 (2011).

    Article  CAS  Google Scholar 

  89. M. Akhtar and P. Jones, Appl. Microbiol. Biotechnol., 78, 853 (2008).

    Article  CAS  Google Scholar 

  90. T. Flynn, M. L. Ghirardi and M. Seibert, Int. J. Hydrog. Energy, 27, 1421 (2002).

    Article  CAS  Google Scholar 

  91. H. McTavish, L.A. Sayavedra-Soto and D. J. Arp, J. Bacteriol., 177, 3960 (1995).

    CAS  Google Scholar 

  92. S. C. E. Tosatto, S. Toppo, C. Donatella, G.M. Giacometti and P. Costantini, Int. J. Hydrog. Energy, 33, 570 (2008).

    Article  CAS  Google Scholar 

  93. M. Ludwig, J. A. Cracknell, K. A. Vincent, F. A. Armstrong and O. Lenz, J. Biol. Chem., 284, 465 (2009).

    Article  CAS  Google Scholar 

  94. S. Dementin, F. Leroux, L. Cournac, A. L. de Lacey, A. Volbeda, C. Léger, B. Burlat, N. Martinez, S. Champ, L. Martin, O. Sanganas, M. Haumann, V.M. Fernández, B. Guigliarelli, J. Fontecilla-Camps and M. Rousset, J. Am. Chem. Soc., 131, 10156 (2009).

    Article  CAS  Google Scholar 

  95. P. P. Liebgott, A. de Lacey, B. Burlat, L. Cournac, P. Richaud, M. Brugna, V. Fernandez, B. Guigliarelli, M. Rousset, C. Léger and S. Dementin, J. Am. Chem. Soc., 133, 986 (2011).

    Article  CAS  Google Scholar 

  96. M. Guiral, P. Tron, V. Belle, C. Aubert, C. Léger and B. Guigliarelli, Int. J. Hydrog. Energy, 31, 1424 (2006).

    Article  CAS  Google Scholar 

  97. J. Y. H. Kim, B. H. Jo and H. J. Cha, Microb. Cell Fact., 9, 54 (2010).

    Article  CAS  Google Scholar 

  98. T. Goris, A. F. Wait, M. Saggu, J. Fritsch, N. Heidary, M. Stein, I. Zebger, F. Lendzian, F. A. Armstrong, B. Friedrich and O. Lenz, Nat. Chem. Biol., 7, 310 (2011).

    Article  CAS  Google Scholar 

  99. R. Mertens and A. Liese, Curr. Opin. Biotechnol., 15, 343 (2004).

    Article  CAS  Google Scholar 

  100. M. Ihara, H. Nishihara, K. S. Yoon, O. Lenz, B. Friedrich, H. Nakamoto, K. Kojima, D. Honma, T. Kamachi and I. Okura, Photochem. Photobiol., 82, 676 (2006).

    Article  CAS  Google Scholar 

  101. H. Krassen, A. Schwarze, B. Friedrich, K. Ataka, O. Lenz and J. Heberle, ACS Nano, 3, 4055 (2009).

    Article  CAS  Google Scholar 

  102. C.E. Lubner, P. Knörzer, P. J. Silva, K. A. Vincent, T. Happe, D. A. Bryant and J. H. Golbeck, Biochemistry, 49, 10264 (2010).

    Article  CAS  Google Scholar 

  103. A.A. Karyakin, S.V. Morozov, E. E. Karyakina, N. A. Zorin, V.V. Perelygin and S. Cosnier, Biochem. Soc. Trans., 33, 73 (2005).

    Article  CAS  Google Scholar 

  104. J.W. Tye, M.B. Hall and M.Y. Darensbourg, Proc. Natl. Acad. Sci. USA, 102, 16911 (2005).

    Article  CAS  Google Scholar 

  105. M. Hambourger, M. Gervaldo, D. Svedruzic, P.W. King, D. Gust, M. Ghirardi, A. L. Moore and T.A. Moore, J. Am. Chem. Soc., 130, 2015 (2008).

    Article  CAS  Google Scholar 

  106. E. Reisner, J.C. Fontecilla-Camps and F. A. Armstrong, Chem. Comm., 5, 550 (2009).

    Article  CAS  Google Scholar 

  107. D. L. Arnon, M. Losada, M. Nozaki and K. Tagawa, Nature, 190, 601 (1961).

    Article  CAS  Google Scholar 

  108. M. Winkler, S. Kuhlgert, M. Hippler and T. Happe, J. Biol. Chem., 284, 36620 (2009).

    Article  CAS  Google Scholar 

  109. J.Y.H. Kim, B.H. Jo, Y. Jo and H. J. Cha, Microb. Cell Fact., 11, 2 (2012).

    Article  CAS  Google Scholar 

  110. S. McGlynn, S. Ruebush, A. Naumov, L. Nagy, A. Dubini, P. King, J. Broderick, M. Posewitz and J.W. Peters, J. Biol. Inorg. Chem., 12, 443 (2007).

    Article  CAS  Google Scholar 

  111. M. E. Boyer, J.A. Stapleton, J. M. Kuchenreuther, C.W. Wang and J. R. Swartz, Biotechnol. Bioeng., 99, 59 (2008).

    Article  CAS  Google Scholar 

  112. J. Sun, R.C. Hopkins, F.E. Jenney, P. M. McTernan and M.W.W. Adams, PLoS ONE, 5, e10526 (2010).

    Article  CAS  Google Scholar 

  113. J. D. Weyman, W. A. Vargas, Y. Tong, J. Yu and P. Maness, PLoS ONE, 6, e20126 (2011).

    Article  CAS  Google Scholar 

  114. M. A. Wells, J. Mercer, R. A. Mott, A.G. Pereira-Medrano, A. M. Burja, H. Radianingtyas and P.C. Wright, Metab. Eng., 13, 445 (2011).

    Article  CAS  Google Scholar 

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Kim, J.Y.H., Cha, H.J. Recent progress in hydrogenase and its biotechnological application for viable hydrogen technology. Korean J. Chem. Eng. 30, 1–10 (2013). https://doi.org/10.1007/s11814-012-0208-8

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