Electronic structure of the unique [4Fe-3S] cluster in O 2-tolerant hydrogenases characterized by 57Fe Mössbauer and EPR spectroscopy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 2, 2013, Pages 483-488

  Pandelia, Maria Eirini ^a   Bykov, Dmytro ^a   Izsak, Robert ^a   Infossi, Pascale ^b   Giudici Orticoni, Marie Thér̀ese ^b   Bill, Eckhard ^a   Neese, Frank ^a   Lubitz, Wolfgang ^a  

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

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4FE 3S PROTEIN; HYDROGENASE; IRON SULFUR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DENSITY FUNCTIONAL THEORY; ELECTRON SPIN RESONANCE; MOSSBAUER SPECTROSCOPY; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION;

AMINO ACID SEQUENCE; BACTERIA; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; HYDROGENASE; IRON; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; SEQUENCE ALIGNMENT; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTROSCOPY, MOSSBAUER; SULFUR;

AQUIFEX AEOLICUS;

EID: 84872194321     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1202575110     Document Type: Article

References (39)

1. Volbeda A, et al. (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373(6515):580-587.
2. Beinert H (2000) Iron-sulfur proteins: Ancient structures, still full of surprises. J Biol Inorg Chem 5(1):2-15.
3. Pandelia ME, et al. (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 USA 108(15):6097-6102.
4. Shomura Y, Yoon KS, Nishihara H, Higuchi Y (2011) Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. Nature 479(7372):253-256.
5. Fritsch J, et al. (2011) The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479(7372):249-252.
6. Lukey MJ, et al. (2011) Oxygen-tolerant [NiFe]-hydrogenases: The individual and collective importance of supernumerary cysteines at the proximal Fe-S cluster. J Am Chem Soc 133(42):16881-16892.
7. 2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli. Proc Natl Acad Sci USA 109(14):5305-5310.
8. Goris T, et al. (2011) A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nat Chem Biol 7(5):310-318.
9. 2)-tolerance? Biochim Biophys Acta 1817(9):1565-1575.
10. Dey A, et al. (2007) Solvent tuning of electrochemical potentials in the active sites of HiPIP versus ferredoxin. Science 318(5855):1464-1468.
11. Niu SQ, Ichiye T (2009) Cleavage of [4Fe-4S]-type clusters: Breaking the symmetry. J Phys Chem A 113(19):5710-5717.
12. Heering HA, Bulsink YB, Hagen WR, Meyer TE (1995) Reversible super-reduction of the cubane [4Fe-4S](3+;2+;1+) in the high-potential iron-sulfur protein under non-denaturing conditions. EPR spectroscopic and electrochemical studies. Eur J Biochem 232(3):811-817.
13. Solomon EI, Xie XJ, Dey A (2008) Mixed valent sites in biological electron transfer. Chem Soc Rev 37(4):623-638.
14. Noodleman L, Peng CY, Case DA, Mouesca JM (1995) Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters. Coord Chem Rev 144:199-244.
15. Beinert H, Holm RH, Münck E (1997) Iron-sulfur clusters: Nature's modular, multipurpose structures. Science 277(5326):653-659.
16. Lippard SJ, Berg JM (1994) Principles of Bioinorganic Chemistry (University Science Books, Mill Valley, CA).
17. Yoon KS, Fukuda K, Fujisawa K, Nishihara H (2011) 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 36:7081-7088.
18. ]2+/3+ high-potential iron-sulfur protein from Chromatium vinosum. Biochemistry 27:8712-8719.
19. Walters EM, et al. (2009) Role of histidine-86 in the catalytic mechanism of ferredoxin: thioredoxin reductase. Biochemistry 48(5):1016-1024.
20. Mouesca JM, Lamotte B (1998) Iron-sulfur clusters and their electronic and magnetic properties. Coord Chem Rev 178:1573-1614.
21. Hamann N, et al. (2009) The CCG-domain-containing subunit SdhE of succinate:quinone oxidoreductase from Sulfolobus solfataricus P2 binds a [4Fe-4S] cluster. J Biol Inorg Chem 14(3):457-470.
22. Middleton P, Dickson DPE, Johnson CE, Rush JD (1980) Interpretation of the Mössbauer spectra of the high-potential iron protein from Chromatium. Eur J Biochem 104(1):289-296.
23. Teixeira M, et al. (1989) Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. Mössbauer and EPR characterization of the metal centers. J Biol Chem 264(28):16435-16450.
24. Huynh BH, et al. (1987) On the active sites of the [NiFe] hydrogenase from Desulfovibrio gigas. Mössbauer and redox-titration studies. J Biol Chem 262(2):795-800.
25. Surerus KK, et al. (1994) Further characterization of the spin coupling observed in oxidized hydrogenase from Chromatium vinosum. A Mössbauer and multifrequency EPR study. Biochemistry 33(16):4980-4993.
26. Schünemann V, Winkler H (2000) Structure and dynamics of biomolecules studied by Mössbauer spectroscopy. Rep Prog Phys 63:263-353.
27. Mouesca JM, Noodleman L, Case DA, Lamotte B (1995) Spin-densities and spin coupling in iron-sulfur clusters - a new analysis of hyperfine coupling-constants. Inorg Chem 34:4347-4359.
28. Cammack R, Patil DS, Fernandez VM (1985) Electron-spin-resonance/ electron-paramagnetic-resonance spectroscopy of iron-sulphur enzymes. Biochem Soc Trans 13(3):572-578.
29. Kent TA, Huynh BH, Münck E (1980) Iron-sulfur proteins: Spin-coupling model for three-iron clusters. Proc Natl Acad Sci USA 77(11):6574-6576.
30. Krebs C, Broderick WE, Henshaw TF, Broderick JB, Huynh BH (2002) 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(6):912-913.
31. 2+ clusters - preparation of clusters with 5-coordinate and 6-coordinate subsites and modulation of redox potentials and charge-distributions. J Am Chem Soc 112:2654-2664.
32. 2+ center with unusual coordination sphere in the LytB protein. J Am Chem Soc 131(37):13184-13185.
33. 3+ cluster in proteins - the importance of double exchange parameter. Z Naturforsch A 50:75-80.
34. Kurtz DM (1990) Oxo-bridged and hydroxo-bridged diiron complexes - A chemical perspective on a biological unit. Chem Rev 90:585-606.
35. Peters JW, et al. (1997) Redox-dependent structural changes in the nitrogenase Pcluster. Biochemistry 36(6):1181-1187.
36. Huang WJ, et al. (1997) Crystal structure of nitrile hydratase reveals a novel iron centre in a novel fold. Structure 5(5):691-699.
37. Popescu VC, et al. (2001) Mössbauer and EPR studies of the photoactivation of nitrile hydratase. Biochemistry 40(27):7984-7991.
38. More C, et al. (2005) Study of the spin-spin interactions between the metal centers of Desulfovibrio gigas aldehyde oxidoreductase: Identification of the reducible sites of the [2Fe-2S]1+,2+ clusters. Biochemistry 44(34):11628-11635.
39. Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430-1436.