Evolution and diversification of Group 1 [NiFe] hydrogenases. Is there a phylogenetic marker for O2-tolerance?

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 9, 2012, Pages 1565-1575

  Pandelia, Maria Eirini ^a   Lubitz, Wolfgang ^a   Nitschke, Wolfgang ^b  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

NiFe hydrogenases; Bioenergetics; Iron sulfur cluster; O2 tolerance; Phylogenetic tree

Indexed keywords

CYSTEINE; HYDROGENASE; IRON; OXYGEN; SULFUR;

AQUIFEX AEOLICUS; ARTICLE; COMPLEX FORMATION; CRENARCHAEOTA; ENZYME STRUCTURE; EURYARCHAEOTA; GENE CLUSTER; GENE DUPLICATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PHYLOGENY; PRIORITY JOURNAL; PROTEOBACTERIA;

ENERGY METABOLISM; HYDROGENASE; IRON-SULFUR PROTEINS; MULTIGENE FAMILY; OXIDATION-REDUCTION; OXYGEN; PHYLOGENY;

EID: 84862223771     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.04.012     Document Type: Article

References (68)

1. N. Lane, J.F. Allen, and W. Martin How did LUCA make a living? Chemiosmosis in the origin of life Bioessays 32 2010 271 280
2. W. Nitschke, and M.J. Russell Hydrothermal focusing of chemical and chemiosmotic energy, supported by delivery of catalytic Fe, Ni, Mo/W, Co, S and Se, forced life to emerge J. Mol. Evol. 69 2009 481 496
3. A.L. Ducluzeau, R. van Lis, S. Duval, B. Schoepp-Cothenet, M.J. Russell, and W. Nitschke Was nitric oxide the first deep electron sink? Trends Biochem. Sci. 34 2009 9 15
4. P.M. Vignais, and B. Billoud Occurrence, classification, and biological function of hydrogenases: an overview Chem. Rev. 107 2007 4206 4272 (Pubitemid 350041744)
5. M. Brugna-Guiral, P. Tron, W. Nitschke, K.O. Stetter, B. Burlat, B. Guigliarelli, M. Bruschi, and M.T. Giudici-Orticoni [NiFe] hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function, and phylogenetics Extremophiles 7 2003 145 157 (Pubitemid 40924484)
6. R.K. Thauer, A.K. Kaster, H. Seedorf, W. Buckel, and R. Hedderich Methanogenic archaea: ecologically relevant differences in energy conservation Nat. Rev. Microbiol. 6 2008 579 591
7. G. Voordouw Evolution of hydrogenase genes Adv. Inorg. Chem. 38 1992 397 422
8. M.E. Pandelia, V. Fourmond, P. Tron-Infossi, E. Lojou, P. Bertrand, C. Leger, M.T. Giudici-Orticoni, and W. Lubitz Membrane-Bound hydrogenase I from the hyperthermophilic bacterium Aquifex aeolicus: enzyme activation, redox intermediates and oxygen tolerance J. Am. Chem. Soc. 132 2010 6991 7004
9. G. Goldet, A.F. Wait, J.A. Cracknell, K.A. Vincent, M. Ludwig, O. Lenz, B. Friedrich, and F.A. Armstrong Hydrogen production under aerobic conditions by membrane-bound hydrogenases from Ralstonia species J. Am. Chem. Soc. 130 2008 11106 11113
10. Y. Shomura, K.S. Yoon, H. Nishihara, and Y. Higuchi Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase Nature 479 2011 253 256
11. M.J. Lukey, A. Parkin, M.M. Roessler, B.J. Murphy, J. Harmer, T. Palmer, F. Sargent, and F.A. Armstrong How Escherichia coli is equipped to oxidize hydrogen under different redox conditions J. Biol. Chem. 285 2010 3928 3938
12. 2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 109 2012 5305 5310
13. A. Volbeda, M.H. Charon, C. Piras, E.C. Hatchikian, M. Frey, and J.C. FontecillaCamps Crystal-structure of the nickel-iron hydrogenase from Desulfovibrio gigas Nature 373 1995 580 587
14. J. Fritsch, P. Scheerer, S. Frielingsdorf, S. Kroschinsky, B. Friedrich, O. Lenz, and C.M.T. Spahn The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre Nature 479 2011 249 252
15. M.E. Pandelia, W. Nitschke, P. Infossi, M.T. Giudici-Orticoni, E. Bill, and W. Lubitz Characterization of a unique [FeS] cluster in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus Proc. Natl. Acad. Sci. U. S. A. 108 2011 6097 6102
16. 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 A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase Nat. Chem. Biol. 7 2011 (p. 310-U87)
17. M.J. Lukey, M.M. Roessler, A. Parkin, R.M. Evans, R.A. Davies, O. Lenz, B. Friedrich, F. Sargent, and F.A. Armstrong Oxygen-tolerant [NiFe]-hydrogenases: the individual and collective importance of supernumerary cysteines at the proximal Fe-S cluster J. Am. Chem. Soc. 133 2011 16881 16892
18. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
19. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 28 2011 2731 2739
20. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The protein data bank Nucleic Acids Res. 28 2000 235 242 (Pubitemid 30047768)
21. N.R. Hackett, and P.D. Bragg The association of 2 distinct b-cytochromes with the respiratory nitrate reductase of Escherichia coli FEMS Microbiol. Lett. 13 1982 213 217 (Pubitemid 12143911)
22. A.L. Ballard, and S.J. Ferguson Respiratory nitrate reductase from Paracoccus denitrificans - evidence for 2 b-type hemes in the gamma-subunit and properties of a water-soluble active enzyme containing alpha-subunit and beta-subunit Eur. J. Biochem. 174 1988 207 212
23. P. Infossi, E. Lojou, J.P. Chauvin, G. Herbette, M. Brugna, and M.T. Giudici-Orticoni Aquifex aeolicus membrane hydrogenase for hydrogen biooxidation: role of lipids and physiological partners in enzyme stability and activity Int. J. Hydrogen Energy 35 2010 10778 10789
24. R. Gross, J. Simon, F. Theis, and A. Kroger Two membrane anchors of Wolinella succinogenes hydrogenase and their function in fumarate and polysulfide respiration Arch. Microbiol. 170 1998 50 58 (Pubitemid 28313867)
25. M. Jormakka, S. Tornroth, B. Byrne, and S. Iwata Molecular basis of proton motive force generation: structure of formate dehydrogenase-N Science 295 2002 1863 1868 (Pubitemid 34214117)
26. L.S. Palagyi-Meszaros, J. Maroti, D. Latinovics, T. Balogh, E. Klement, K.F. Medzihradszky, G. Rakhely, and K.L. Kovacs Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS FEBS J. 276 2009 164 174
27. F.D. Ciccarelli, T. Doerks, C. von Mering, C.J. Creevey, B. Snel, and P. Bork Toward automatic reconstruction of a highly resolved tree of life Science 311 2006 1283 1287 (Pubitemid 43334717)
28. F. Baymann, E. Lebrun, M. Brugna, B. Schoepp-Cothenet, M.T. Giudici-Orticoni, and W. Nitschke The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 267 274 (Pubitemid 36178235)
29. M. Jormakka, K. Yokoyama, T. Yano, M. Tamakoshi, S. Akimoto, T. Shimamura, P. Curmi, and S. Iwata Molecular mechanism of energy conservation in polysulfide respiration Nat. Struct. Mol. Biol. 15 2008 730 737 (Pubitemid 351931998)
30. A. Dubini, R.L. Pye, R.L. Jack, T. Palmer, and F. Sargent How bacteria get energy from hydrogen: a genetic analysis of periplasmic hydrogen oxidation in Escherichia coli Int. J. Hydrogen Energy 27 2002 1413 1420
31. N.K. Menon, C.Y. Chatelus, M. Dervartanian, J.C. Wendt, K.T. Shanmugam, H.D. Peck, and A.E. Przybyla Cloning, sequencing, and mutational analysis of the Hyb-operon encoding Escherichia coli hydrogenase-2 J. Bacteriol. 176 1994 4416 4423 (Pubitemid 24226480)
32. B. Schoepp-Cothenet, C. Lieutaud, F. Baymann, A. Vermeglio, T. Friedrich, D.M. Kramer, and W. Nitschke Menaquinone as pool quinone in a purple bacterium Proc. Natl. Acad. Sci. U. S. A. 106 2009 8549 8554
33. T.V. Laurinavichene, and A.A. Tsygankov The involvement of hydrogenases 1 and 2 in the hydrogen-dependent nitrate respiration of Escherichia coli Microbiology 72 2003 654 659 (Pubitemid 39009076)
34. M. Teixeira, I. Moura, A.V. Xavier, J.J.G. Moura, J. LeGall, D.V. Der Vartanian, H.D. Peck, and B.H. Huynh Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen - Mössbauer and EPR characterization of the metal centers J. Biol. Chem. 264 1989 16435 16450
35. H. Miyadera, A. Hiraishi, H. Miyoshi, K. Sakamoto, R. Mineki, K. Murayama, K.V.P. Nagashima, K. Matsuura, S. Kojima, and K. Kita Complex II from phototrophic purple bacterium Rhodoferax fermentans displays rhodoquinol-fumarate reductase activity Eur. J. Biochem. 270 2003 1863 1874 (Pubitemid 36534484)
36. B.C. Brajcich, A.L. Iarocci, L.A.G. Johnstone, R.K. Morgan, Z.T. Lonjers, M.J. Hotchko, J.D. Muhs, A. Kieffer, B.J. Reynolds, S.M. Mandel, B.N. Marbois, C.F. Clarke, and J.N. Shepherd Evidence that ubiquinone is a required intermediate for rhodoquinone biosynthesis in Rhodospirillum rubrum J. Bacteriol. 192 2010 436 445
37. G.J. Mander, E.C. Duin, D. Linder, K.O. Stetter, and R. Hedderich Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea Eur. J. Biochem. 269 2002 1895 1904 (Pubitemid 34429671)
38. F. Grein, I.A.C. Pereira, and C. Dahl Biochemical characterization of individual components of the Allochromatium vinosum DsrMKJOP transmembrane complex aids understanding of complex function in vivo J. Bacteriol. 192 2010 6369 6377
39. M.G. Bertero, R.A. Rothery, M. Palak, C. Hou, D. Lim, F. Blasco, J.H. Weiner, and N.C.J. Strynadka Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A Nat. Struct. Biol. 10 2003 681 687 (Pubitemid 37052404)
40. R. Hedderich, N. Hamann, and M. Bennati Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster Biol. Chem. 386 2005 961 970 (Pubitemid 41548728)
41. R.H. Pires, S.S. Venceslau, F. Morais, M. Teixeira, A.V. Xavier, and I.A.C. Pereira Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex - a membrane-bound redox complex involved in the sulfate respiratory pathway Biochemistry 45 2006 249 262 (Pubitemid 43054985)
42. N. Hamann, G.J. Mander, J.E. Shokes, R.A. Scott, M. Bennati, and R. Hedderich Cysteine-rich CCG domain contains a novel [4Fe-4S] cluster binding motif as deduced from studies with subunit B of heterodisulfide reductase from Methanothermobacter marburgensis Biochemistry 46 2007 12875 12885 (Pubitemid 350060108)
43. J.M.C.C. Coremans, C.J. Vangarderen, and S.P.J. Albracht On the redox equilibrium between H-2 and hydrogenase Biochim. Biophys. Acta 1119 1992 148 156
44. H. Ogata, P. Kellers, and W. Lubitz The crystal structure of the [NiFe] hydrogenase from the photosynthetic bacterium Allochromatium vinosum: characterization of the oxidized enzyme (Ni-A state) J. Mol. Biol. 402 2010 428 444
45. B. Bleijlevens, F.A. van Broekhuizen, A.L. De Lacey, W. Roseboom, V.M. Fernandez, and S.P.J. Albracht The activation of the [NiFe]-hydrogenase from Allochromatium vinosum. An infrared spectro-electrochemical study J. Biol. Inorg. Chem. 9 2004 743 752 (Pubitemid 39279252)
46. K. Knüttel, K. Schneider, A. Erkens, W. Plass, A. Muller, E. Bill, and A.X. Trautwein Redox properties of the metal centers in the membrane-bound hydrogenase from Alcaligenes eutrophus CH34 Bull. Pol. Acad. Sci., Chem. 42 1994 495 511
47. M. Tietze, A. Beuchle, I. Lamla, N. Orth, M. Dehler, G. Greiner, and U. Beifuss Redox potentials of methanophenazine and CoB-S-S-CoM, factors involved in electron transport in methanogenic archaea Chem. Biochem. 4 2003 333 335 (Pubitemid 36505202)
48. R. Gross, R. Pisa, M. Sanger, C.R.D. Lancaster, and J. Simon Characterization of the menaquinone reduction site in the diheme cytochrome b membrane anchor of Wolinella succinogenes NiFe-hydrogenase J. Biol. Chem. 279 2004 274 281 (Pubitemid 38044825)
49. U. Beifuss, M. Tietze, S. Baumer, and U. Deppenmeier Methanophenazine: structure, total synthesis, and function of a new cofactor from methanogenic archaea Angew. Chem. Int. Ed. 39 2000 2470
50. W.A. Vargas, P.D. Weyman, Y.K. Tong, H.O. Smith, and Q. Xu [NiFe] Hydrogenase from Alteromonas macleodii with unusual stability in the presence of oxygen and high temperature Appl. Environ. Microbiol. 77 2011 1990 1998
51. K. Schneider, D.S. Patil, and R. Cammack Electron-spin-resonance properties of membrane-bound hydrogenases from aerobic hydrogen bacteria Biochim. Biophys. Acta 748 1983 353 361
52. K. Knüttel, K. Schneider, H.G. Schlegel, and A. Muller The membrane-bound hydrogenase from Paracoccus denitrificans - purification and molecular characterization Eur. J. Biochem. 179 1989 101 108 (Pubitemid 19097664)
53. R. Cammack, V.M. Fernandez, and E.C. Hatchikian Nickel-iron hydrogenase Inorg. Microb. Sulfur Metabol. 243 1994 43 68
54. J.H. Sun, and D.J. Arp Aerobically purified hydrogenase from Azotobacter vinelandii - activity, activation, and spectral properties Arch. Biochem. Biophys. 287 1991 225 233
55. K.S. Yoon, N. Tsukada, Y. Sakai, M. Ishii, Y. Igarashi, and H. Nishihara Isolation and characterization of a new facultatively autotrophic hydrogen-oxidizing betaproteobacterium, Hydrogenophaga sp AH-24 FEMS Microbiol. Lett. 278 2008 94 100 (Pubitemid 350215889)
56. K.S. Yoon, K. Fukuda, K. Fujisawa, and H. Nishihara Purification and characterization of a highly thermostable, oxygen-resistant, respiratory [NiFe]-hydrogenase from a marine, aerobic hydrogen-oxidizing bacterium Hydrogenovibrio marinus Int. J. Hydrogen Energy 36 2011 7081 7088
57. M. Saggu, I. Zebger, M. Ludwig, O. Lenz, B. Friedrich, P. Hildebrandt, and F. Lendzian Spectroscopic insights into the oxygen-tolerant membrane-associated [NiFe] hydrogenase of Ralstonia eutropha H16 J. Biol. Chem. 284 2009 16264 16276
58. B. Boussau, L. Gueguen, and M. Gouy Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of aquificales in the phylogeny of bacteria BMC Evol. Biol. 8 2008 272
59. W. Nitschke, R. van Lis, B. Schoepp-Cothenet, and F. Baymann The green phylogenetic clade of Rieske/cytb complexes Photosynth. Res. 104 2010 347 355
60. T.V. Laurinavichene, and A.A. Tsygankov H-2 consumption by Escherichia coli coupled via hydrogenase 1 or hydrogenase 2 to different terminal electron acceptors FEMS Microbiol. Lett. 202 2001 121 124 (Pubitemid 32744802)
61. E.M. Shepard, E.S. Boyd, J.B. Broderick, and J.W. Peters Biosynthesis of complex iron-sulfur enzymes Curr. Opin. Chem. Biol. 15 2011 319 327
62. M. Fontecave, and S. Ollagnier-de-Choudens Iron-sulfur cluster biosynthesis in bacteria: mechanisms of cluster assembly and transfer Arch. Biochem. Biophys. 474 2008 226 237
63. J. Fritsch, O. Lenz, and B. Friedrich The maturation factors HoxR and HoxT contribute to oxygen tolerance of membrane-bound [NiFe] hydrogenase in Ralstonia eutropha H16 J. Bacteriol. 193 2011 2487 2497
64. B.M. Wolfe, S.M. Lui, H. Manyani, L. Rey, J.M. Palacios, J. Imperial, and T. Ruiz-Argueso Gene products of the hupGHIJ Operon are involved in maturation of the iron-sulfur subunit of the [NiFe] hydrogenase from Rhizobium leguminosarum bv. viciae J. Bacteriol. 187 2005 7018 7026 (Pubitemid 41428878)
65. L.A. Sazanov, and P. Hinchliffe Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus Science 311 2006 1430 1436 (Pubitemid 43376691)
66. S. Sham, L. Calzolai, P.L. Wang, K. Bren, H. Haarklau, P.S. Brereton, M.W.W. Adams, and G.N. La Mar A solution NMR molecular model for the aspartate-ligated, cubane cluster containing ferredoxin from the hyperthermophilic archeaon Pyrococcus furiosus Biochemistry 41 2002 12498 12508
67. (2 +) cluster of Bacillus subtilis transcriptional regulator Fnr J. Biol. Chem. 286 2011 2017 2021
68. O. Schröder, B. Bleijlevens, T.E. de Jongh, Z.J. Chen, T.S. Li, J. Fischer, J. Forster, C.G. Friedrich, K.A. Bagley, S.P.J. Albracht, and W. Lubitz Characterization of a cyanobacterial-like uptake [NiFe] hydrogenase: EPR and FTIR spectroscopic studies of the enzyme from Acidithiobacillus ferrooxidans J. Biol. Inorg. Chem. 12 2007 212 233 (Pubitemid 46197946)