Radical AdoMet enzymes in complex metal cluster biosynthesis

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 11, 2012, Pages 1254-1263

  Duffus, Benjamin R ^a   Hamilton, Trinity L ^a   Shepard, Eric M ^a   Boyd, Eric S ^a   Peters, John W ^a   Broderick, Joan B ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

Biosynthesis; Hydrogenase; Iron sulfur cluster; Nitrogenase; Radical S adenosylmethionine enzyme; Scaffold protein

Indexed keywords

AMINO ACID; ENZYME; INORGANIC COMPOUND; IRON HYDROGENASE; IRON SULFUR PROTEIN; NITROGENASE; RADICAL S ADENOSYLMETHIONINE ENZYME; S ADENOSYLMETHIONINE; SCAFFOLD PROTEIN; SULFUR; UNCLASSIFIED DRUG;

CATALYST; CHEMICAL MODIFICATION; CHEMICAL REACTION; COMPLEX FORMATION; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

BACTERIAL PROTEINS; BIOCATALYSIS; COORDINATION COMPLEXES; EVOLUTION, MOLECULAR; FREE RADICALS; HYDROGENASE; IRON; IRON-SULFUR PROTEINS; MODELS, MOLECULAR; MOLYBDOFERREDOXIN; NITROGENASE; PHYLOGENY; S-ADENOSYLMETHIONINE; SULFUR;

EID: 84866024911     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.01.002     Document Type: Review

References (97)

1. G. Wächtershäuser From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya Philos. Trans. R. Soc. London, Ser. B 361 2006 1787 1808
2. W. Martin, and M.J. Russell On the origin of biochemistry at an alkaline hydrothermal vent Philos. Trans. R. Soc. London, Ser. B 362 2007 1887 1925
3. 2 + via homogeneous and heterogeneous reactions - part 1: evaluation of aqueous photochemical, prebiotic pathways Origins Life Evol. Biosphere 38 2008 127 137
4. 2 for reduction; a requirement for both pre-biotic and biological mechanisms Origins Life Evol. Biosphere 38 2008 195 209
5. 2 redox couple as reductant Origins Life Evol. Biosphere 29 1999 5 32
6. N.N. Nair, E. Schreiner, and D. Marx Glycine at the pyrite-water interface: the role of surface defects J. Am. Chem. Soc. 128 2006 13815 13826
7. (I)-S phase on pyrite by atomic hydrogen beam surface reactive scattering Langmuir 27 2011 6814 6821
8. D.J. Berrisford, C. Bolm, and K.B. Sharpless Ligand-accelerated catalysis Angew. Chem. Int. Ed Engl. 34 1995 1059 1070
9. G. Wächtershäuser On the chemistry and evolution of the pioneer organism Chem. Biodivers. 4 2007 584 602
10. S.E. McGlynn, D.W. Mulder, E.M. Shepard, J.B. Broderick, and J.W. Peters Hydrogenase cluster biosynthesis: organometallic chemistry nature's way Dalton Trans. 2009 4274 4285
11. H. Beinert, R.H. Holm, and E. Munck Iron-sulfur clusters: nature's modular, multipurpose structures Science 277 1997 653 659
12. H. Beinert Iron-sulfur proteins: ancient structures, still full of surprises J. Biol. Inorg. Chem. 5 2000 2 15
13. D.C. Johnson, D.R. Dean, A.D. Smith, and M.K. Johnson Structure, function, and formation of biological iron-sulfur clusters Annu. Rev. Biochem. 74 2005 247 281
14. J.C. Fontecilla-Camps, P. Amara, C. Cavazza, Y. Nicolet, and A. Volbeda Structure-function relationships of anaerobic gas-processing metalloenzymes Nature 460 2009 814 822
15. D.C. Rees, and J.B. Howard The interface between the biological and inorganic worlds: iron-sulfur metalloclusters Science 300 2003 929 931
16. 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
17. J.W. Peters, W.N. Lanzilotta, B.J. Lemon, and L.C. Seefeldt X-ray crystal structure of the Fe-only hydrogenase (Cpl) from Clostridium pasteurianum to 1.8 angstrom resolution Science 282 1998 1853 1858
18. Y. Nicolet, C. Piras, P. Legrand, C.E. Hatchikian, and J.C. Fontecilla-Camps Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center Structure 7 1999 13 23
19. 14N HYSCORE investigation of the H-cluster of [FeFe] hydrogenase: evidence for a nitrogen in the dithiol bridge Phys. Chem. Chem. Phys. 11 2009 6592 6599
20. Y. Nicolet, B.J. Lemon, J.C. Fontecilla-Camps, and J.W. Peters A novel FeS cluster in Fe-only hydrogenases Trends Biochem. Sci. 25 2000 138 143
21. Y. Nicolet, C. Cavazza, and J.C. Fontecilla-Camps Fe-only hydrogenases: structure, function and evolution J. Inorg. Biochem. 91 2002 1 8
22. A.S. Pandey, T.V. Harris, L.J. Giles, J.W. Peters, and R.K. Szilagyi Dithiomethylether as a ligand in the hydrogenase H-cluster J. Am. Chem. Soc. 130 2008 4533 4540
23. U. Ryde, C. Greco, and L. De Gioia Quantum refinement of [FeFe] hydrogenase indicates a dithiomethylamine ligand J. Am. Chem. Soc. 132 2010 4512 4513
24. D.W. Mulder, E.M. Shepard, J.E. Meuser, N. Joshi, P.W. King, M.C. Posewitz, J.B. Broderick, and J.W. Peters Insights into [FeFe]-hydrogenase structure, mechanism, and maturation Structure 19 2011 1038 1052
25. D.W. Mulder, D.O. Ortillo, D.J. Gardenghi, A.V. Naumov, S.S. Ruebush, R.K. Szilagyi, B. Huynh, J.B. Broderick, and J.W. Peters Activation of HydA(Delta EFG) requires a preformed [4Fe-4S] cluster Biochemistry 48 2009 6240 6248
26. D.W. Mulder, E.S. Boyd, R. Sarma, R.K. Lange, J.A. Endrizzi, J.B. Broderick, and J.W. Peters Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydA(Delta EFG) Nature 465 2010 248 251
27. J.W. Peters, and R.K. Szilagyi Exploring new frontiers of nitrogenase structure and mechanism Curr. Opin. Chem. Biol. 10 2006 101 108
28. L.M. Rubio, and P.W. Ludden Biosynthesis of the iron-molybdenum cofactor of nitrogenase Annu. Rev. Microbiol. 62 2008 93 111
29. T.R. Hoover, A.D. Robertson, R.L. Cerny, R.N. Hayes, J. Imperial, V.K. Shah, and P.W. Ludden Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate Nature 329 1987 855 857
30. O. Einsle, F.A. Tezcan, S.L.A. Andrade, B. Schmid, M. Yoshida, J.B. Howard, and D.C. Rees Nitrogenase MoFe-protein at 1.16 Å resolution: a central ligand in the FeMo-cofactor Science 297 2002 1696 1700
31. B. Schmid, M.W. Ribbe, O. Einsle, M. Yoshida, L.M. Thomas, D.R. Dean, D.C. Rees, and B.K. Burgess Structure of a cofactor-deficient nitrogenase MoFe protein Science 296 2002 352 356
32. 2 activation Chem. Rec. 7 2007 37 46
33. 2 Arch. Microbiol. 169 1998 206 210
34. 2-forming methylenetetrahydromethanopterin dehydrogenase (Hmd) and of HmdII and HmdIII in Methanothermobacter marburgensis Arch. Microbiol. 174 2000 225 232
35. 2 storage Annu. Rev. Biochem. 79 2010 507 536
36. S. Shima, O. Pilak, S. Vogt, M. Schick, M.S. Stagni, W. Meyer-Klaucke, E. Warkentin, R.K. Thauer, and U. Ermler The crystal structure of [Fe]-hydrogenase reveals the geometry of the active site Science 321 2008 572 575
37. T. Hiromoto, K. Ataka, O. Pilak, S. Vogt, M.S. Stagni, W. Meyer-Klaucke, E. Warkentin, R.K. Thauer, S. Shima, and U. Ermler The crystal structure of C176A mutated [Fe]-hydrogenase suggests an acyl-iron ligation in the active site iron complex FEBS Lett. 583 2009 585 590
38. H.J. Sofia, G. Chen, B.G. Hetzler, J.F. Reyes-Spindola, and N.E. Miller Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods Nucleic Acids Res. 29 2001 1097 1106
39. C. Krebs, W.E. Broderick, T.F. Henshaw, J.B. Broderick, and B.H. Huynh Coordination of adenosylmethionine to a unique iron site of the [4Fe-4S] of pyruvate formate-lyase activating enzyme: a Mössbauer spectroscopic study J. Am. Chem. Soc. 124 2002 912 913
40. + cluster of pyruvate formate-lyase activating enzyme J. Am. Chem. Soc. 124 2002 3143 3151
41. C.J. Walsby, D. Ortillo, W.E. Broderick, J.B. Broderick, and B.M. Hoffman An anchoring role for FeS clusters: chelation of the amino acid moiety of S-adenosylmethionine to the unique iron site of the [4Fe-4S] cluster of pyruvate formate-lyase activating enzyme J. Am. Chem. Soc. 124 2002 11270 11271
42. D. Chen, C. Walsby, B.M. Hoffman, and P.A. Frey Coordination and mechanism of reversible cleavage of S-adenosylmethionine by the [4Fe-4S] center in lysine 2,3-aminomutase J. Am. Chem. Soc. 125 2003 11788 11789
43. 1 + cluster of pyruvate formate-lyase activating enzyme generates the glycyl radical on pyruvate formate-lyase: EPR-detected single turnover J. Am. Chem. Soc. 122 2000 8331 8332
44. 2+/1 + in lysine 2,3-aminomutase Biochemistry 45 2006 3219 3225
45. S.C. Wang, and P.A. Frey Binding energy in the one-electron reductive cleavage of S-adenosylmethionine in lysine 2,3-aminomutase, a radical SAM enzyme Biochemistry 46 2007 12889 12895
46. Y. Nicolet, P. Amara, J.-M. Mouesca, and J.C. Fontecilla-Camps Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins Proc. Natl. Acad. Sci. U. S. A. 106 2009 14867 14871
47. E.M. Shepard, and J.B. Broderick S-adenosylmethionine and iron-sulfur clusters in biological radical reactions: The radical SAM superfamily L. Mander, H.-W. Liu, Comprehensive Natural Products Chemistry vol. 8 2010 Elsevier Oxford 625 661
48. M.C. Posewitz, P.W. King, S.L. Smolinski, L. Zhang, M. Seibert, and M.L. Ghirardi Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase J. Biol. Chem. 279 2004 25711 25720
49. J. Meyer [FeFe] hydrogenases and their evolution: a genomic perspective Cell. Mol. Life Sci. 64 2007 1063 1084
50. A. Böck, P.W. King, M. Blokesch, and M.C. Posewitz Maturation of hydrogenases Adv. Microb. Physiol. 51 2006 1 71
51. P.W. King, M.C. Posewitz, M.L. Ghirardi, and M. Seibert Functional studies of [FeFe] hydrogenase maturation in an Escherichia coli biosynthetic system J. Bacteriol. 188 2006 2163 2172
52. T.P. Begley, D.M. Downs, S.E. Ealick, F.W. McLafferty, A.P.G.M. Van Loon, S. Taylor, N. Campobasso, H.-J. Chiu, C. Kinsland, J.J. Reddick, and J. Xi Thiamin biosynthesis in prokaryotes Arch. Microbiol. 171 1999 293 300
53. T.P. Begley Cofactor biosynthesis: an organic chemist's treasure trove Nat. Prod. Rep. 23 2006 15 25
54. M. Kriek, F. Martins, M.R. Challand, A. Croft, and P.L. Roach Thiamine biosynthesis in Escherichia coli: identification of the intermediate and by-product derived from tyrosine Angew. Chem. Int. Ed. 46 2007 9223 9226
55. E. Pilet, Y. Nicolet, C. Mathevon, T. Douki, J.C. Fontecilla-Camps, and M. Fontecave The role of the maturase HydG in [FeFe]-hydrogenase active site synthesis and assembly FEBS Lett. 583 2009 506 511
56. J.M. Kuchenreuther, J.A. Stapleton, and J.R. Swartz Tyrosine, cysteine, and S-adenosyl methionine stimulate in vitro [FeFe] hydrogenase activation PLoS One 4 2009 e7565
57. Y. Nicolet, J.K. Rubach, M.C. Posewitz, P. Amara, C. Mathevon, M. Atta, M. Fontecave, and J.C. Fontecilla-Camps X-ray structure of the [FeFe]-hydrogenase maturase HydE from Thermotoga maritima J. Biol. Chem. 283 2008 18861 18872
58. R.C. Driesener, M.R. Challand, S.E. McGlynn, E.M. Shepard, E.S. Boyd, J.B. Broderick, J.W. Peters, and P.L. Roach [FeFe]-hydrogenase cyanide ligands derived from S-adenosylmethionine-dependent cleavage of tyrosine Angew. Chem. Int. Ed. 49 2010 1687 1690
59. E.M. Shepard, B.R. Duffus, S.J. George, S.E. McGlynn, M.R. Challand, K.D. Swanson, P.L. Roach, S.P. Cramer, J.W. Peters, and J.B. Broderick [FeFe]-hydrogenase maturation: HydG-catalyzed synthesis of carbon monoxide J. Am. Chem. Soc. 132 2010 9247 9249
60. E. Antonini, and M. Brunori Hemoglobin and Myoglobin in Their Reactions with Ligands 1971 North Holland Publishing Amsterdam
61. -ligands derive from tyrosine PLoS One 6 2011 e20346
62. J.K. Rubach, X. Brazzolotto, J. Gaillard, and M. Fontecave Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima FEBS Lett. 579 2005 5055 5060
63. Y. Nicolet, L. Martin, C. Tron, and J.C. Fontecilla-Camps A glycyl free radical as the precursor in the synthesis of carbon monoxide and cyanide by the [FeFe]-hydrogenase maturase HydG FEBS Lett. 584 2010 4197 4202
64. C. Tron, M.V. Cherrier, P. Amara, L. Martin, F. Fauth, E. Fraga, M. Correard, M. Fontecave, Y. Nicolet, and J.C. Fontecilla-Camps Further characterization of the [FeFe]-hydrogenase maturase HydG Eur. J. Inorg. Chem. 2011 1121 1127
65. P.L. Roach Radicals from S-adenosylmethionine and their application to biosynthesis Curr. Opin. Chem. Biol. 15 2011 267 275
66. J.W. Peters, R.K. Szilagyi, A. Naumov, and T. Douglas A radical solution for the biosynthesis of the H-cluster of hydrogenase FEBS Lett. 580 2006 363 367
67. E.M. Shepard, S.E. McGlynn, A.L. Bueling, C.S. Grady-Smith, S.J. George, M.A. Winslow, S.P. Cramer, J.W. Peters, and J.B. Broderick Synthesis of the 2Fe subcluster of the [FeFe]-hydrogenase H cluster on the HydF scaffold Proc. Natl. Acad. Sci. U. S. A. 107 2010 10448 10453
68. J.L. Vey, and C.L. Drennan Structural insights into radical generation by the radical SAM superfamily Chem. Rev. 111 2011 2487 2506
69. X. Brazzolotto, J.K. Rubach, J. Gaillard, S. Gambarelli, M. Atta, and M. Fontecave The [Fe-Fe]-hydrogenase maturation protein HydF from Thermotoga maritima is a GTPase with an iron-sulfur cluster J. Biol. Chem. 281 2006 769 774
70. S.E. McGlynn, S.S. Ruebush, A. Naumov, L.E. Nagy, A. Dubini, P.W. King, J.B. Broderick, M.C. Posewitz, and J.W. Peters In vitro activation of [FeFe] hydrogenase: new insights into hydrogenase maturation J. Biol. Inorg. Chem. 12 2007 443 447
71. S.E. McGlynn, E.M. Shepard, M.A. Winslow, A.V. Naumov, K.S. Duschene, M.C. Posewitz, W.E. Broderick, J.B. Broderick, and J.W. Peters HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis FEBS Lett. 582 2008 2183 2187
72. B.K. Burgess, and D.J. Lowe Mechanism of molybdenum nitrogenase Chem. Rev. 96 1996 2983 3012
73. L. Curatti, P.W. Ludden, and L.M. Rubio NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase Proc. Natl. Acad. Sci. U. S. A. 103 2006 5297 5301
74. S. Tal, T.W. Chun, N. Gavini, and B.K. Burgess The delta nifB (or delta nifE) FeMo cofactor-deficient MoFe protein is different from the delta nifH protein J. Biol. Chem. 266 1991 10654 10657
75. P.C. Dos Santos, D.R. Dean, Y. Hu, and M.W. Ribbe Formation and insertion of the nitrogenase iron-molybdenum cofactor Chem. Rev. 104 2004 1159 1173
76. E.S. Boyd, A.D. Anbar, S. Miller, T.L. Hamilton, M. Lavin, and J.W. Peters A late methanogen origin for molybdenum-dependent nitrogenase Geobiology 9 2011 221 232
77. J.A. Hernandez, R.Y. Igarashi, B. Soboh, L. Curatti, D.R. Dean, P.W. Ludden, and L.M. Rubio NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway Mol. Microbiol. 63 2007 177 192
78. R.D. Joerger, and P.E. Bishop Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii J. Bacteriol. 170 1988 1475 1487
79. V.K. Shah, J.R. Allen, N.J. Spangler, and P.W. Ludden In vitro synthesis of the iron-molybdenum cofactor of nitrogenase - purification and characterization of NifB cofactor, the product of NifB protein J. Biol. Chem. 269 1994 1154 1158
80. S.J. George, R.Y. Igarashi, Y. Xiao, J.A. Hernandez, M. Demuez, D. Zhao, Y. Yoda, P.W. Ludden, L.M. Rubio, and S.P. Cramer Extended X-ray absorption fine structure and nuclear resonance vibrational spectroscopy reveal that NifB-co, a FeMo-co precursor, comprises a 6Fe core with an interstitial light atom J. Am. Chem. Soc. 130 2008 5673 5680
81. G. Schwarz, R.R. Mendel, and M.W. Ribbe Molybdenum cofactors, enzymes and pathways Nature 460 2009 839 847
82. Y. Hu, M.C. Corbett, A.W. Fay, J.A. Webber, K.O. Hodgson, B. Hedman, and M.W. Ribbe FeMo cofactor maturation on NifEN Proc. Natl. Acad. Sci. U. S. A. 103 2006 17119 17124
83. E.S. Boyd, T.L. Hamilton, and J.W. Peters An alternative path for the evolution of biological nitrogen fixation Front. Microbiol. 2 2011 205
84. J.T. Kaiser, Y. Hu, J.A. Wiig, D.C. Rees, and M.W. Ribbe Structure of precursor-bound NifEN: a nitrogenase FeMo cofactor maturase/insertase Science 331 2011 91 94
85. A.W. Fay, M.A. Blank, J.M. Yoshizawa, C.C. Lee, J.A. Wiig, Y. Hu, K.O. Hodgson, B. Hedman, and M.W. Ribbe Formation of a homocitrate-free iron-molybdenum cluster on NifEN: implications for the role of homocitrate in nitrogenase assembly Dalton Trans. 39 2010 3124 3130
86. J.A. Wiig, Y. Hu, and M.W. Ribbe NifEN-B complex of Azotobacter vinelandii is fully functional in nitrogenase FeMo cofactor assembly Proc. Natl. Acad. Sci. U. S. A. 108 2011 8623 8627
87. P. Hänzelmann, and H. Schindelin Binding of 5 ′-GTP to the C-terminal FeS cluster of the radical S-adenosylmethionine enzyme MoaA provides insights into its mechanism Proc. Natl. Acad. Sci. U. S. A. 103 2006 6829 6834
88. C.J. Bult, O. White, G.J. Olsen, L. Zhou, R.D. Fleischmann, G.G. Sutton, J.A. Blake, L.M. FitzGerald, R.A. Clayton, J.D. Gocayne, A.R. Kerlavage, B.A. Dougherty, J.-F. Tomb, M.D. Adams, C.I. Reich, R. Overbeek, E.F. Kirkness, K.G. Weinstock, J.M. Merrick, A. Glodek, J.L. Scott, N.S.M. Geoghagen, J.F. Weidman, J.L. Fuhrmann, D. Nguyen, T.R. Utterback, J.M. Kelley, J.D. Peterson, P.W. Sadow, M.C. Hanna, M.D. Cotton, K.M. Roberts, M.A. Hurst, B.P. Kaine, M. Borodovsky, H.-P. Klenk, C.M. Fraser, H.O. Smith, C.R. Woese, and J.C. Venter Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii Science 273 1996 1058 1073
89. H. Wang, D. Boisvert, K.K. Kim, R. Kim, and S.-H. Kim Crystal structure of a fibrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 1.6 angstrom resolution EMBO J. 19 2000 317 323
90. S.E. McGlynn, E.S. Boyd, E.M. Shepard, R.K. Lange, R. Gerlach, J.B. Broderick, and J.W. Peters Identification and characterization of a novel member of the radical AdoMet enzyme superfamily and implications for the biosynthesis of the Hmd hydrogenase active site cofactor J. Bacteriol. 192 2010 595 598
91. 4 cluster and binds S-adenosylmethionine Mol. Microbiol. 59 2006 795 806
92. N.C. Martinez-Gomez, and D.M. Downs ThiC is an [Fe-S] cluster protein that requires AdoMet to generate the 4-amino-5-hydroxymethyl-2-methylpyrimidine moiety in thiamin synthesis Biochemistry 47 2008 9054 9056
93. Y. Zhang, X. Zhu, A.T. Torelli, M. Lee, B. Dzikovski, R.M. Koralewski, E. Wang, J. Freed, C. Krebs, S.E. Ealick, and H. Lin Diphthamide biosynthesis requires an organic radical generated by an iron-sulphur enzyme Nature 465 2010 891 896
94. S.C. Silver, T. Chandra, E. Zilinskas, S. Ghose, W.E. Broderick, and J.B. Broderick Complete stereospecific repair of a synthetic dinucleotide spore photoproduct by spore photoproduct lyase J. Biol. Inorg. Chem. 15 2010 943 955
95. S.C. Wang, and P.A. Frey S-adenosylmethionine as an oxidant: the radical SAM superfamily Trends Biochem. Sci. 32 2007 101 110
96. Y. Yu, L. Duan, Q. Zhang, R. Liao, Y. Ding, H. Pan, E. Wendt-Pienkowski, G. Tang, B. Shen, and W. Liu Nosiheptide biosynthesis featuring a unique indole side ring formation on the characteristic thiopeptide framework ACS Chem. Biol. 4 2009 855 864
97. Q. Zhang, Y. Li, D. Chen, Y. Yu, L. Duan, B. Shen, and W. Liu Radical-mediated enzymatic carbon chain fragmentation-recombination Nat. Chem. Biol. 7 2011 154 160