Cryo-Elektronenmikroskopie- und Kristallstruktur der F420-reduzierenden [NiFe]-Hydrogenase (FrhABG) aus Methanothermobacter marburgensis

Die Methanbildung aus H2 und CO2 ist die einzige Energie-liefernde Reaktion in vielen methanogenen Archaeen. Pro Mol gebildetem Methan werden vier Mol H2 verbraucht. Der Wasserstoff wird dabei durch Hydrogenasen aktiviert, wovon es in den meisten hydrogenotrophen Methanbildnern drei unterschiedliche...

Full description

Saved in:
Bibliographic Details
Main Author: Vitt, Stella
Contributors: Shima, Seigo (Ph.D.) (Thesis advisor)
Format: Dissertation
Published: Philipps-Universität Marburg 2013
Online Access:PDF Full Text
Tags: Add Tag
No Tags, Be the first to tag this record!

1. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (5259):680-685.

2. Çinkaya, I. 2002. Substrat induzierte Radikalbildung in dem Eisen-Schwefel Flavoenzym 4- Hydroxybutyryl-CoA-Dehydratase aus Clostridium aminobutyricum

3. Smith, E. T., J. M. Tomich, T. Iwamoto, J. H. Richards, Y. Mao, and B. A. Feinberg. 1991. A totally synthetic histidine-2 ferredoxin: thermal stability and redox properties. Biochemistry 30 (50):11669-11676.

4. Vignais und Billoud, B. 2007. Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107 (10):4206-4272.

5. Schönheit, P., J. Moll, and R. K. Thauer. 1980. Growth parameters (Ks, mmax, Ys) of Methanobacterium thermoautotrophicum. Arch. Microbiol. 127:59-65.

6. Sorgenfrei, O., S. Muller, M. Pfeiffer, I. Sniezko, and A. Klein. 1997b. The [NiFe] hydrogenases of Methanococcus voltae: genes, enzymes and regulation. Arch Microbiol 167 (4):189-195.

7. Vaupel und Thauer, R. K. 1998. Two F420-reducing hydrogenases in Methanosarcina barkeri. Arch Microbiol 169 (3):201-205.

8. Afting, C., A. Hochheimer, and R. K. Thauer. 1998. Function of H2-forming methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum in coenzyme F420 reduction with H2. Archives of Microbiology 169 (3):206-210.

9. Beinert, H. 2000a. Iron-sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5 (1):2- 15.

10. Albracht, S. P. 1994. Nickel hydrogenases: in search of the active site. Biochim Biophys Acta 1188 (3):167- 204.

11. Menon, N. K., J. Robbins, M. Der Vartanian, D. Patil, H. D. Peck, Jr., A. L. Menon, R. L. Robson, and A. E. Przybyla. 1993. Carboxy-terminal processing of the large subunit of [NiFe] hydrogenases. FEBS Lett 331 (1-2):91-95.

12. Asso, G., Yagi, Bertrand. 1992. EPR and redox properties of Desulfovibrio vulgaris Miyazaki hydrogenase- comparison with the [NiFe] enzyme from Desulfovibrio gigas. Biochim Biophys Acta 1122:50-56.

13. Aufhammer, S. W., E. Warkentin, H. Berk, S. Shima, R. K. Thauer, and U. Ermler. 2004. Coenzyme binding in F420-dependent secondary alcohol dehydrogenase, a member of the bacterial luciferase family. Structure 12 (3):361-370.

14. Dutta und Berman, H. M. 2005. Large macromolecular complexes in the Protein Data Bank: a status report. Structure 13 (3):381-388.

15. Teshima, T., A. Nakaji, T. Shiba, L. Tsai, and S. Yamazaki. 1985. Elucidation of Stereospecificity of a Selenium-Containing Hydrogenase from Methanococcus vannielii -Synthesis of (R) and (S)-[4-2h1]- 3,4-Dihydro-7-Hydroxy-1-Hydroxyethylquinolinone. Tetrahedron Letters 26 (3):351-354.

16. Voordouw, G. 1992. Evolution of Hydrogenase Genes. Advances in Inorganic Chemistry 38:397-422.

17. Higuchi, Y., T. Yagi, and N. Yasuoka. 1997. Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 5 (12):1671-1680.

18. Higuchi, Y., H. Ogata, K. Miki, N. Yasuoka, and T. Yagi. 1999. Removal of the bridging ligand atom at the Ni-Fe active site of [NiFe] hydrogenase upon reduction with H2, as revealed by X-ray structure analysis at 1.4 Å resolution. Structure 7 (5):549-556.

19. Ceh, K., U. Demmer, E. Warkentin, J. Moll, R. K. Thauer, S. Shima, and U. Ermler. 2009. Structural basis of the hydride transfer mechanism in F420-dependent methylenetetrahydromethanopterin dehydrogenase. Biochemistry 48 (42):10098-10105.

20. Sumner und Matthews, R. 1992. Stereochemistry and mechanism of hydrogen transfer between NADPH and methylenetetrahydrofolate in the reaction catalyzed by methylenetetrahydrofolate reductase from pig liver. J Am Chem Soc 114:6949-6956.

21. Muraki, N., J. Nomata, K. Ebata, T. Mizoguchi, T. Shiba, H. Tamiaki, G. Kurisu, and Y. Fujita. 2010. X- ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465 (7294):110-114.

22. Baker, M. L., J. Zhang, S. J. Ludtke, and W. Chiu. 2010. Cryo-EM of macromolecular assemblies at near- atomic resolution. Nat Protoc 5 (10):1697-1708.

23. Bingemann und Klein, A. 2000a. Conversion of the central [4Fe-4S] cluster into a [3Fe-4S] cluster leads to reduced hydrogen-uptake activity of the F420-reducing hydrogenase of Methanococcus voltae. European Journal of Biochemistry 267 (22):6612-6618.

24. Bitto, E., C. A. Bingman, L. Bittova, D. A. Kondrashov, R. M. Bannen, B. G. Fox, J. L. Markley, and G. N. Phillips, Jr. 2008. Structure of human J-type co-chaperone HscB reveals a tetracysteine metal- binding domain. J Biol Chem 283 (44):30184-30192.

25. Bryson, K., L. J. McGuffin, R. L. Marsden, J. J. Ward, J. S. Sodhi, and D. T. Jones. 2005. Protein structure prediction servers at University College London. Nucleic Acids Res 33 (Web Server issue):W36- 38.

26. Imai, T., K. Taguchi, Y. Ogawara, D. Ohmori, F. Yamakura, H. Ikezawa, and A. Urushiyama. 2001. Characterization and cloning of an extremely thermostable, Pyrococcus furiosus-type 4Fe ferredoxin from Thermococcus profundus. J Biochem 130 (5):649-655.

27. Armstrong und Albracht, S. P. 2005. [NiFe]-hydrogenases: spectroscopic and electrochemical definition of reactions and intermediates. Philos Transact A Math Phys Eng Sci 363 (1829):937-954; discussion 1035-1040.

28. Potterton, E., S. McNicholas, E. Krissinel, K. Cowtan, and M. Noble. 2002. The CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 58 (Pt 11):1955-1957.

29. Dautant, A., J. B. Meyer, J. Yariv, G. Precigoux, R. M. Sweet, A. J. Kalb, and F. Frolow. 1998. Structure of a monoclinic crystal from of cyctochrome b1 (Bacterioferritin) from E. coli. Acta Crystallogr D Biol Crystallogr 54 (Pt 1):16-24.

30. Aufhammer, S. W., E. Warkentin, U. Ermler, C. H. Hagemeier, R. K. Thauer, and S. Shima. 2005. Crystal structure of methylenetetrahydromethanopterin reductase (Mer) in complex with coenzyme F420: Architecture of the F420/FMN binding site of enzymes within the nonprolyl cis-peptide containing bacterial luciferase family. Protein Sci 14 (7):1840-1849.

31. Fiebig und Friedrich, B. 1989. Purification of the F420-reducing hydrogenase from Methanosarcina barkeri (strain Fusaro). Eur J Biochem 184 (1):79-88.

32. Constant, P., S. P. Chowdhury, L. Hesse, J. Pratscher, and R. Conrad. 2011. Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H2-oxidizing bacteria. Appl Environ Microbiol 77 (17):6027-6035.

33. Kaster, A. K., M. Goenrich, H. Seedorf, H. Liesegang, A. Wollherr, G. Gottschalk, and R. K. Thauer. 2011a. More than 200 genes required for methane formation from H2 and CO2 and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus. Archaea 2011:973848.

34. You, K. S. 1985. Stereospecificity for nicotinamide nucleotides in enzymatic and chemical hydride transfer reactions. CRC Crit Rev Biochem 17 (4):313-451.

35. Sutter, M., D. Boehringer, S. Gutmann, S. Gunther, D. Prangishvili, M. J. Loessner, K. O. Stetter, E. Weber-Ban, and N. Ban. 2008. Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat Struct Mol Biol 15 (9):939-947.

36. Daniel und Danson, M. J. 1995. Did primitive microorganisms use nonhem iron proteins in-place of NAD/P. Journal of Molecular Evolution 40 (6):559-563.

37. Sorgenfrei, O., E. C. Duin, A. Klein, and S. P. Albracht. 1997a. Changes in the electronic structure around Ni in oxidized and reduced selenium-containing hydrogenases from Methanococcus voltae. Eur J Biochem 247 (2):681-687.

38. Gipson, P., D. J. Mills, R. Wouts, M. Grininger, J. Vonck, and W. Kuhlbrandt. 2010. Direct structural insight into the substrate-shuttling mechanism of yeast fatty acid synthase by electron cryomicroscopy. Proceedings of the National Academy of Sciences of the United States of America 107 (20):9164-9169.

39. Johansson, P., B. Wiltschi, P. Kumari, B. Kessler, C. Vonrhein, J. Vonck, D. Oesterhelt, and M. Grininger. 2008. Inhibition of the fungal fatty acid synthase type I multienzyme complex. Proc Natl Acad Sci U S A 105 (35):12803-12808.

40. Brunger, A. T. 1992. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355 (6359):472-475.

41. Böck, A., P. W. King, M. Blokesch, and M. C. Posewitz. 2006. Maturation of hydrogenases. Adv Microb Physiol 51:1-71.

42. Massanz, C., S. Schmidt, and B. Friedrich. 1998. Subforms and in vitro reconstitution of the NAD- reducing hydrogenase of Alcaligenes eutrophus. J Bacteriol 180 (5):1023-1029.

43. Valente, F. M., A. S. Oliveira, N. Gnadt, I. Pacheco, A. V. Coelho, A. V. Xavier, M. Teixeira, C. M. Soares, and I. A. Pereira. 2005. Hydrogenases in Desulfovibrio vulgaris Hildenborough: structural and physiologic characterisation of the membrane-bound [NiFeSe] hydrogenase. J Biol Inorg Chem 10 (6):667-682.

44. Janda und Hemmerich, P. 1976. 5-deaza-thiariboflavins and 5-thiariboflavins -simple pathway to antietabolites of vitamine B2 Angewandte Chemie-International Edition in English 15 (7):443- 444. Literaturverzeichnis 106 106

45. Keweloh. 1980. Abbau von Faktor F420 in Methanobacterium thermoautotrophicum bei Einwirkung von O2. . Diploma thesis, Philips-Universität, Marburg.

46. Nakos, M. u. 1973. Bacterial ferredoxins and /or iron sulfur proteins as electron carriers. Lovenberg W (ed) Iron Sulfur Proteins. Academic Press, New York: pp 37–64.

47. Michel, R., C. Massanz, S. Kostka, M. Richter, and K. Fiebig. 1995a. Biochemical characterization of the 8-hydroxy-5-deazaflavin-reactive hydrogenase from Methanosarcina barkeri Fusaro. Eur J Biochem 233 (3):727-735.

48. Thauer, R. K. 1998. Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology 144 ( Pt 9):2377-2406.

49. Oelgeschlager und Rother, M. 2008. Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea. Arch Microbiol 190 (3):257-269.

50. Alex, L. A., J. N. Reeve, W. H. Ormejohnson, and C. T. Walsh. 1990a. Cloning, Sequence determination and Expression of the Genes encoding the Subunits of the Nickel-containing 8-Hydroxy-5- Deazaflavine reducing Hydrogenase from Methanobaczerium thermoautrophicum Delta-H Biochemistry 29 (31):7237-7244.

51. Liesegang, H., A. K. Kaster, A. Wiezer, M. Goenrich, A. Wollherr, H. Seedorf, G. Gottschalk, and R. K. Thauer. 2010. Complete genome sequence of Methanothermobacter marburgensis, a methanoarchaeon model organism. J Bacteriol 192 (21):5850-5851.

52. Fang, B., M. Kim, J. H. Kim, and J. S. Yu. 2008. Controllable synthesis of hierarchical nanostructured hollow core/mesopore shell carbon for electrochemical hydrogen storage. Langmuir 24 (20):12068-12072.

53. Tamada, T., K. Kitadokoro, Y. Higuchi, K. Inaka, A. Yasui, P. E. de Ruiter, A. P. Eker, and K. Miki. 1997. Crystal structure of DNA photolyase from Anacystis nidulans. Nat Struct Biol 4 (11):887-891.

54. Ein unheimlich großer Dank geht an meine Familie, für ihre unermessliche Unterstützung in all den durchlebten Lebenslagen, ihren unermüdlichen Bemühungen und dem liebevollen Rückhalt – ohne sie wäre dies alles nie möglich gewesen.

55. Marcus, R. A. 1956a. Electrostatic Free Energy and Other Properties of States Having Nonequilibrium Polarization I. J.Chem.Phys. 24 (979).

56. Tang, G., L. Peng, P. R. Baldwin, D. S. Mann, W. Jiang, I. Rees, and S. J. Ludtke. 2007. EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157 (1):38-46.

57. Ludtke, S. J., P. R. Baldwin, and W. Chiu. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128 (1):82-97.

58. Buckel und Thauer, R. K. 2012. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na (+) translocating ferredoxin oxidation. Biochim Biophys Acta.

59. Montet, Y., P. Amara, A. Volbeda, X. Vernede, E. C. Hatchikian, M. J. Field, M. Frey, and J. C. Fontecilla- Camps. 1997. Gas access to the active site of [NiFe] hydrogenases probed by X-ray crystallography and molecular dynamics. Nat Struct Biol 4 (7):523-526.

60. Garcin, E., X. Vernede, E. C. Hatchikian, A. Volbeda, M. Frey, and J. C. Fontecilla-Camps. 1999. The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Structure with Folding & Design 7 (5):557-566.

61. Volbeda, A., Y. Montet, X. Vernede, E. C. Hatchikian, and J. C. Fontecilla-Camps. 2002. High-resolution crystallographic analysis of Desulfovibrio fructiosovorans [NiFe] hydrogenase. International Journal of Hydrogen Energy 27 (11-12):1449-1461.

62. Volbeda, A., L. Martin, C. Cavazza, M. Matho, B. W. Faber, W. Roseboom, S. P. J. Albracht, E. Garcin, M. Rousset, and J. C. Fontecilla-Camps. 2005. Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. Journal of Biological Inorganic Chemistry 10 (3):239-249.

63. Volbeda, A., P. Amara, C. Darnault, J. M. Mouesca, A. Parkin, M. M. Roessler, F. A. Armstrong, and J. C. Fontecilla-Camps. 2012. X-ray crystallographic and computational studies of the O2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli. Proc Natl Acad Sci U S A 109 (14):5305-5310.

64. Rousset, M., Y. Montet, B. Guigliarelli, N. Forget, M. Asso, P. Bertrand, J. C. Fontecilla-Camps, and E. C. Hatchikian. 1998. [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis. Proc Natl Acad Sci U S A 95 (20):11625-11630.

65. Forschungsaufenthalt an der Universität von

66. Atmosphäre im Labor. Hervorzuheben sei hier Dr. Michael Schick mit seiner stetigen Hilfsbereitschaft beim Gasflaschen anschließen, Sachen suchen, und seiner teilweise strapazierfähigen Nerven.

67. Hydrogenase without a Bridging Ligand in the Active Site in Its Oxidised, "as-Isolated" State. Journal of Molecular Biology 396 (4):893-907.

68. Taylor, M. C., C. J. Jackson, D. B. Tattersall, N. French, T. S. Peat, J. Newman, L. J. Briggs, G. V. Lapalikar, P. M. Campbell, C. Scott, R. J. Russell, and J. G. Oakeshott. 2010. Identification and characterization of two families of F420H2-dependent reductases from Mycobacteria that catalyse aflatoxin degradation. Mol Microbiol 78 (3):561-575.

69. Bei Dr. Janet Vonck vom Max-Planck-Institut für Biophysik in Frankfurt a.M. möchte ich mich für die gute und sehr nette Zusammenarbeit bei der Cryo-EM Struktur und für das Korrigieren des " Cryo-EM-

70. Page, C. C., C. C. Moser, X. Chen, and P. L. Dutton. 1999. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402 (6757):47-52.

71. Matias, P. M., C. M. Soares, L. M. Saraiva, R. Coelho, J. Morais, J. Le Gall, and M. A. Carrondo. 2001. [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three- dimensional structure determination and refinement at 1.8 Å and modelling studies of its interaction with the tetrahaem cytochrome c3. J Biol Inorg Chem 6 (1):63-81.

72. Marcus, R. A. 1956b. On the Theory of Oxidation-Reduction Reactions Involving Electron Transfer I.

73. PD Dr. Antonio J. Pierik gilt mein Dank für gemeinsamen Stunden während der ESR-Messungen, für die ESR-Messungen und die Auswertungen.

74. Muth, E., E. Morschel, and A. Klein. 1987a. Purification and characterization of an 8-hydroxy-5- deazaflavin-reducing hydrogenase from the archaebacterium Methanococcus voltae. Eur J Biochem 169 (3):571-577.

75. Jacobson, F. S., L. Daniels, J. A. Fox, C. T. Walsh, and W. H. Ormejohnson. 1982a. Purification and properties of an 8-Hydroxy-5-Deazaflavin-reducing Hydrogenase from Methanobacterium thermoautotrophicum Journal of Biological Chemistry 257 (7):3385-3388.

76. Baron und Ferry, J. G. 1989a. Purification and properties of the membrane-associated coenzyme F420- reducing hydrogenase from Methanobacterium formicicum. J Bacteriol 171 (7):3846-3853.

77. Teixeira, M., I. Moura, A. V. Xavier, J. J. Moura, J. LeGall, D. V. DerVartanian, H. D. Peck, Jr., and B. H. Huynh. 1989. Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. Mossbauer and EPR characterization of the metal centers. J Biol Chem 264 (28):16435- 16450.

78. Knüttel. 1994. Redox properties of the metal centers in the membrane-bound hydrogenase from Alcaligenes aquifexaeolicus eutrophus CH34. . Bull Pol Acad Sci Chem 42:495-511.

79. Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53 (Pt 3):240-255.

80. Dym und Eisenberg, D. 2001. Sequence-structure analysis of FAD-containing proteins. Protein Sci 10 (9):1712-1728.

81. Lebenslauf Name: Stella Vitt Geburtsdatum: 07. Februar 1984, in Siegen Familienstand: verheiratet, ein Kind (geboren am: 19. Februar 2012)

82. Saeki, M. u. 1992. Structural and functional diversity of ferredoxins and related proteins. Cammack R, Sykes AG (eds) Advances in inorganic chemistry 38 ( Academic Press, San Diego):223–280.

83. Shomura, Y., K. S. Yoon, H. Nishihara, and Y. Higuchi. 2011. Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. Nature.

84. Guerlesquin, B. u. 1988. Structure, function and evolution of bacterial ferredoxins. FEMS Microbiol Rev 4 (2):155-175.

85. Boisvert, D. C., J. Wang, Z. Otwinowski, A. L. Horwich, and P. B. Sigler. 1996. The 2.4 A crystal structure of the bacterial chaperonin GroEL complexed with ATP gamma S. Nat Struct Biol 3 (2):170-177.

86. Adman, S. u. 2001. The 2[4Fe-4S] ferredoxins. Messerschmidt A, Huber R, Poulos T, Wieghardt K (eds) Hand-book of metalloproteins. Wiley, Chichester:574–592.

87. Parkin, A., G. Goldet, C. Cavazza, J. C. Fontecilla-Camps, and F. A. Armstrong. 2008. The difference a Se makes? Oxygen-tolerant hydrogen production by the [NiFeSe]-hydrogenase from Desulfomicrobium baculatum. J Am Chem Soc 130 (40):13410-13416.

88. Harrison und Arosio, P. 1996. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275 (3):161-203.

89. Schwarz und Friedrich, B. 2003. The H2-metabolizing prokaryotes. In The prokaryotes: An evolving electronic resource for the microbiological community. Edited by M. Dworkin et al. New York: Springer.

90. DeLano, W. L. 2002. The Pymol User's Manual. .

91. Marques, M. C., R. Coelho, A. L. De Lacey, I. A. Pereira, and P. M. Matias. 2010. The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidised, "as-isolated" state. J Mol Biol 396 (4):893-907.

92. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem 25 (13):1605-1612.

93. Überaus dankbar bin ich auch PD Dr. Ulrich Ermler vom Max-Planck-Institut für Biophysik in Frankfurt a.M., für die unzähligen Stunden die wir mit Kristallpicken und vermessen verbracht haben. Für die Möglichkeit in Villigen, Schweiz, gewesen zu sein und für seine große Mühe und Ruhe mich ein wenig in die Strukturaufklärung einzuführen, mir den Modellbau zu erklären, für das Korrigieren des " Kristall- Teils " dieser Arbeit und die Beantwortung all meiner Fragen.

94. Diplomarbeit an der Goethe Universität Frankfurt a. M. in der Arbeitsgruppe von Prof. Dr. Volker Müller: " Untersuchungen zur Caffeatatmung in Acetobacterium woodii " Juni 2007–Februar 2008

95. Kabsch, W. 2010. Xds. Acta Crystallogr D Biol Crystallogr 66 (Pt 2):125-132.

96. Thamer, W., I. Cirpus, M. Hans, A. J. Pierik, T. Selmer, E. Bill, D. Linder, and W. Buckel. 2003. A two [4Fe-4S]-cluster-containing ferredoxin as an alternative electron donor for 2-hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans. Arch Microbiol 179 (3):197-204.

97. Theodoratou, E., R. Huber, and A. Bock. 2005. [NiFe]-Hydrogenase maturation endopeptidase: structure and function. Biochem Soc Trans 33 (Pt 1):108-111.

98. Calzolai, L., C. M. Gorst, Z. H. Zhao, Q. Teng, M. W. Adams, and G. N. La Mar. 1995. 1H NMR investigation of the electronic and molecular structure of the four-iron cluster ferredoxin from the hyperthermophile Pyrococcus furiosus. Identification of Asp14 as a cluster ligand in each of the four redox states. Biochemistry 34 (36):11373-11384.

99. Fox, J. A., D. J. Livingston, W. H. Orme-Johnson, and C. T. Walsh. 1987. 8-Hydroxy-5-deazaflavin- reducing hydrogenase from Methanobacterium thermoautotrophicum: 1. Purification and characterization. Biochemistry 26 (14):4219-4227.

100. Eirich, L. D., G. D. Vogels, and R. S. Wolfe. 1978. Proposed structure for coenzyme F420 from Methanobacterium. Biochemistry 17 (22):4583-4593.

101. Bruggemann, H., F. Falinski, and U. Deppenmeier. 2000. Structure of the F420H2:quinone oxidoreductase of Archaeoglobus fulgidus identification and overproduction of the F420H2-oxidizing subunit. Eur J Biochem 267 (18):5810-5814.

102. Bahadur, R. P., P. Chakrabarti, F. Rodier, and J. Janin. 2003. Dissecting subunit interfaces in homodimeric proteins. Proteins 53 (3):708-719.

103. Schuwirth, B. S., M. A. Borovinskaya, C. W. Hau, W. Zhang, A. Vila-Sanjurjo, J. M. Holton, and J. H. Cate. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310 (5749):827-834.

104. Schneider und Sheldrick, G. M. 2002. Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58 (Pt 10 Pt 2):1772-1779.

105. Emsley und Cowtan, K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 (Pt 12 Pt 1):2126-2132.

106. Padilla und Yeates, T. O. 2003. A statistic for local intensity differences: robustness to anisotropy and pseudo-centering and utility for detecting twinning. Acta Crystallogr D Biol Crystallogr 59 (Pt 7):1124-1130.

107. Urich, T., C. M. Gomes, A. Kletzin, and C. Frazao. 2006. X-ray Structure of a self-compartmentalizing sulfur cycle metalloenzyme. Science 311 (5763):996-1000.

108. Thauer, R. K., A. K. Kaster, M. Goenrich, M. Schick, T. Hiromoto, and S. Shima. 2010. Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu Rev Biochem 79:507- 536.

109. Fritsch, J., P. Scheerer, S. Frielingsdorf, S. Kroschinsky, B. Friedrich, O. Lenz, and C. M. Spahn. 2011. The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature.

110. Ogata, H., P. Kellers, and W. Lubitz. 2010. The Crystal Structure of the [NiFe] Hydrogenase from the Photosynthetic Bacterium Allochromatium vinosum: Characterization of the Oxidized Enzyme (Ni-A State). Journal of Molecular Biology 402 (2):428-444.

111. Johnson und Mukhopadhyay, B. 2005. A new type of sulfite reductase, a novel coenzyme F420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii. J Biol Chem 280 (46):38776-38786.

112. Bashiri, G., C. J. Squire, N. J. Moreland, and E. N. Baker. 2008. Crystal structures of F420-dependent glucose-6-phosphate dehydrogenase FGD1 involved in the activation of the anti-tuberculosis drug candidate PA-824 reveal the basis of coenzyme and substrate binding. J Biol Chem 283 (25):17531-17541.

113. Volbeda, A., M. H. Charon, C. Piras, E. C. Hatchikian, M. Frey, and J. C. Fontecillacamps. 1995. Crystal- Structure of the Nickel-Iron Hydrogenase from Desulfovibrio gigas. Nature 373 (6515):580-587.

114. Scheres und Chen, S. 2012. Prevention of overfitting in cryo-EM structure determination. Nat Methods 9 (9):853-854.

115. Thauer, R. K., A. K. Kaster, H. Seedorf, W. Buckel, and R. Hedderich. 2008. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6 (8):579-591.

116. Urich, T., T. M. Bandeiras, S. S. Leal, R. Rachel, T. Albrecht, P. Zimmermann, C. Scholz, M. Teixeira, C. M. Gomes, and A. Kletzin. 2004. The sulphur oxygenase reductase from Acidianus ambivalens is a multimeric protein containing a low-potential mononuclear non-haem iron centre. Biochem J 381 (Pt 1):137-146.

117. Warkentin, E., B. Mamat, M. Sordel-Klippert, M. Wicke, R. K. Thauer, M. Iwata, S. Iwata, U. Ermler, and S. Shima. 2001. Structures of F420H2:NADP + oxidoreductase with and without its substrates bound. EMBO J 20 (23):6561-6569.

118. Logan, D. T., E. Mulliez, K. M. Larsson, S. Bodevin, M. Atta, P. E. Garnaud, B. M. Sjoberg, and M. Fontecave. 2003. A metal-binding site in the catalytic subunit of anaerobic ribonucleotide reductase. Proc Natl Acad Sci U S A 100 (7):3826-3831.

119. Caffrey, S. M., H. S. Park, J. K. Voordouw, Z. He, J. Zhou, and G. Voordouw. 2007. Function of periplasmic hydrogenases in the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. J Bacteriol 189 (17):6159-6167.

120. Braks, I. J., M. Hoppert, S. Roge, and F. Mayer. 1994. Structural aspects and immunolocalization of the F420-reducing and non-F420-reducing hydrogenases from Methanobacterium thermoautotrophicum Marburg. J Bacteriol 176 (24):7677-7687.

121. Lunsdorf, H., M. Niedrig, and K. Fiebig. 1991. Immunocytochemical localization of the coenzyme F420- reducing hydrogenase in Methanosarcina barkeri Fusaro. J Bacteriol 173 (3):978-984.

122. ———. 1989b. Reconstitution and properties of a coenzyme F420-mediated formate hydrogenlyase system in Methanobacterium formicicum. J Bacteriol 171 (7):3854-3859.

123. Wackett, L., E. Hartwieg, J. King, W. Orme-Johnson, and C. Walsh. 1987a. Electron microscopy of nickel-containing methanogenic enzymes: methyl reductase and F420-reducing hydrogenase. J. Bacteriol. 169:718-727.

124. Baron, S. F., D. P. Brown, and J. G. Ferry. 1987. Locations of the hydrogenases of Methanobacterium formicicum after subcellular fractionation of cell extract. J Bacteriol 169 (8):3823-3825.

125. Conrad, R., M. Aragno, and W. Seiler. 1983. Production and consumption of hydrogen in a eutrophic lake. Appl Environ Microbiol 45 (2):502-510.

126. Kulkarni, G., D. M. Kridelbaugh, A. M. Guss, and W. W. Metcalf. 2009. Hydrogen is a preferred intermediate in the energy-conserving electron transport chain of Methanosarcina barkeri. Proc Natl Acad Sci U S A 106 (37):15915-15920.

127. Zhang, J., M. L. Baker, G. F. Schroder, N. R. Douglas, S. Reissmann, J. Jakana, M. Dougherty, C. J. Fu, M. Levitt, S. J. Ludtke, J. Frydman, and W. Chiu. 2010. Mechanism of folding chamber closure in a group II chaperonin. Nature 463 (7279):379-383.

128. Sun, J., R. C. Hopkins, F. E. Jenney, P. M. McTernan, and M. W. Adams. 2010. Heterologous expression and maturation of an NADP-dependent [NiFe]-hydrogenase: a key enzyme in biofuel production. PLoS One 5 (5):e10526.

129. Wang, S., H. Huang, J. Moll, and R. K. Thauer. 2010. NADP + reduction with reduced ferredoxin and NADP + reduction with NADH are coupled via an electron-bifurcating enzyme complex in Clostridium kluyveri. J Bacteriol 192 (19):5115-5123.

130. Gruner, I., C. Fradrich, L. H. Bottger, A. X. Trautwein, D. Jahn, and E. Hartig. 2011. Aspartate 141 is the fourth ligand of the oxygen-sensing [4Fe-4S] 2+ cluster of Bacillus subtilis transcriptional regulator Fnr. J Biol Chem 286 (3):2017-2021.

131. Kaster, A. K., J. Moll, K. Parey, and R. K. Thauer. 2011b. Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc Natl Acad Sci U S A 108 (7):2981-2986.

132. Pandelia, M. E., W. Nitschke, P. Infossi, M. T. Giudici-Orticoni, E. Bill, and W. Lubitz. 2011. 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 (15):6097-6102.

133. Ge und Zhou, Z. H. 2011. Hydrogen-bonding networks and RNA bases revealed by cryo electron microscopy suggest a triggering mechanism for calcium switches. Proc Natl Acad Sci U S A 108 (23):9637-9642.

134. Welte und Deppenmeier, U. 2011. Membrane-bound electron transport in Methanosaeta thermophila. J Bacteriol 193 (11):2868-2870.

135. Sakai, S., Y. Takaki, S. Shimamura, M. Sekine, T. Tajima, H. Kosugi, N. Ichikawa, E. Tasumi, A. T. Hiraki, A. Shimizu, Y. Kato, R. Nishiko, K. Mori, N. Fujita, H. Imachi, and K. Takai. 2011. Genome sequence of a mesophilic hydrogenotrophic methanogen Methanocella paludicola, the first cultivated representative of the order Methanocellales. PLoS One 6 (7):e22898.

136. Kojima, N., J. A. Fox, R. P. Hausinger, L. Daniels, W. A. Orme-Johnson, and C. Walsh. 1983. Paramagnetic centers in the nickel-containing, deazaflavin reducing hydrogenase from Methanobacterium thermoautotrophicum. Proc. Natl. Acad. Sci USA. 80:378-382.

137. Yamazaki, S., L. Tsai, T. C. Stadtman, T. Teshima, A. Nakaji, and T. Shiba. 1985. Stereochemical studies of a selenium-containing hydrogenase from Methanococcus vannielii: determination of the absolute configuration of C-5 chirally labeled dihydro-8-hydroxy-5-deazaflavin cofactor. Proc Natl Acad Sci U S A 82 (5):1364-1366.

138. Shima et al; Thauer, R. K. 2001. Tetrahydromethanopterin-specific enzymes from Methanopyrus kandleri. Methods Enzymol 331:317-353.

139. Sprott, G. D., K. M. Shaw, and T. J. Beveridge. 1987. Properties of the particluate enzyme F420-reducing hydrogenase isolated from Methanospirillum hungatei. Can. J. Microbiol. 33:896-904.

140. Teixeira, V. H., A. M. Baptista, and C. M. Soares. 2006. Pathways of H2 toward the active site of [NiFe]- hydrogenase. Biophys J 91 (6):2035-2045.

141. Ludtke, S. J., M. L. Baker, D. H. Chen, J. L. Song, D. T. Chuang, and W. Chiu. 2008. De novo backbone trace of GroEL from single particle electron cryomicroscopy. Structure 16 (3):441-448.

142. Ogata, H., W. Lubitz, and Y. Higuchi. 2009. [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism. Dalton Trans (37):7577-7587.

143. Stock, T., M. Selzer, S. Connery, D. Seyhan, A. Resch, and M. Rother. 2011. Disruption and complementation of the selenocysteine biosynthesis pathway reveals a hierarchy of selenoprotein gene expression in the archaeon Methanococcus maripaludis. Mol Microbiol 82 (3):734-747.

144. Dementin, S., V. Belle, P. Bertrand, B. Guigliarelli, G. Adryanczyk-Perrier, A. L. De Lacey, V. M. Fernandez, M. Rousset, and C. Leger. 2006. Changing the ligation of the distal [4Fe4S] cluster in [NiFe] hydrogenase impairs inter-and intramolecular electron transfers. J Am Chem Soc 128 (15):5209-5218.

145. Constant, P., S. P. Chowdhury, J. Pratscher, and R. Conrad. 2010. Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ Microbiol 12 (3):821-829.