How oxygen reacts with oxygen-tolerant respiratory [NiFe]-hydrogenases

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

Volumn 111, Issue 18, 2014, Pages 6606-6611

  Wulff, Philip ^a   Day, Christopher C ^a   Sargent, Frank ^b   Armstrong, Fraser A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Fe S cluster; Hydrogen; Mass spectrometry

Indexed keywords

HYDROGEN; HYDROGEN PEROXIDE; HYDROGENASE 1; HYDROXYLAMINE; NICKEL IRON HYDROGENASE; OXIDOREDUCTASE; OXYGEN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; UNCLASSIFIED DRUG; WATER;

ARTICLE; CYTOPLASM; DECOMPOSITION; ELECTRON; ELECTRON TRANSPORT; ENZYME ACTIVITY; ESCHERICHIA COLI; MASS SPECTROMETRY; NONHUMAN; OXIDATION; PRIORITY JOURNAL;

FE-S CLUSTER; HYDROGEN; MASS SPECTROMETRY;

CATALYTIC DOMAIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN PEROXIDE; HYDROGENASE; MASS SPECTROMETRY; MODELS, MOLECULAR; NICKEL; OXIDOREDUCTASES; OXYGEN; PROTEIN STRUCTURE, QUATERNARY;

EID: 84899819167     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322393111     Document Type: Article

References (46)

1. 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
2. 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. Pr oc Natl Acad Sci USA 108(15):6097-6102
3. Lukey MJ, et al. (2010) How Escherichia coli is equipped to oxidize hydrogen under different redox conditions. J Biol Chem 285(6):3928-3938.
4. Lamle SE, Albracht SPJ, Armstrong FA (2004) Electrochemical potential-step investigations of the aerobic interconversions of [NiFe]-hydrogenase from Allochromatium vinosum: Insights into the puzzling difference bet ween unready and ready oxidized inactive states. J Am Chem Soc 126(45):14899-14909
5. Vincent KA, et al. (2005) Electrochemical definitions of O2 sensitivity and oxidative inactivation in hydrogenases. J Am Chem Soc 127(51):18179-18189
6. Volbeda A, et al. (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10(3):239-249
7. Ogata H, Lubitz W, Higuchi Y (2009) [NiFe] hydrogenases: Structural and spectroscopic studies of the reaction mechanism. Dalton Trans (37):7577-7587
8. Cr acknell JA, Wait AF, Lenz O, Friedrich B, Armstrong FA (2009) A kinetic and thermodynamic understanding of O2 tolerance in [NiFe]-hydrogenases. Proc Natl Acad Sci USA 106(49):20681-20686
9. Evans RM, et al. (2013) Principles of sustained enzymatic hydrogen oxidation in the presence of oxygen-The crucial influence of high potential Fe-S clusters in the electron relay of [NiFe]-hydrogenases. J Am Chem Soc 135(7):2694-2707.
10. Volbeda A et al. 2012, X-ray crystallographic and computational studies of the O2-tolerant [NiFe]-hydrogenase from Escherichia coli. Proc Natl Acad Sci USA 109(14):5305-5310
11. Volbeda A, et al. (2013) Crystal structure of the O(2)-tolerant membrane-bound hydrogenase from Escherichia coli in complex with its cognate cytochrome b. Structure 21(1):184-190
12. Shomura Y, Yoon K-S, 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
13. Fritsch J, et al. (2011) The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479(7372):249-252
14. 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
15. Roessler MM, Evans RM, Davies RA, Harmer J, Armstrong FA (2012) EPR spectroscopic studies of the Fe-S clusters in the O2-tolerant [NiFe]-hydrogenase H yd-1 from Escherichia coli and characterization of the unique [4Fe-3S] cluster by HYSCORE. J Am Chem Soc 134(37):15581-15594
16. Teixeira M, et al. (1989) Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. Mö ssbauer and EPR characterization of the metal centers. J Biol Chem 264(28):16435-16450
17. Lauterbach L, Lenz O (2013) Catalytic production of hydrogen peroxide and water by oxygen-tolerant [NiFe]-hydrogenase during H2 cycling in the presence of O2. J Am Chem Soc 135(47):17897-17905
18. Rousset M, et al. (1998) [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis. Proc Natl Acad Sci USA 95(20):11625-11630
19. Kussmaul L, Hirst J (2006) The mechanism of superoxide production by NADH: Ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci USA 103(20):7607-7612
20. Ba lversWG, Boersma MG, Vervoort J, Rietjens IM (1992) Experimental and theoretical study on the redox cycling of resorufin by solubilized and membrane-bound NADPHcytochrome reductase. Chem Res Toxicol 5(2):268-273.
21. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: A simple assay for superoxide dismutase. Anal Biochem 70(2):616-620
22. Schneider K , Schlegel HG (1981) Production of superoxide radicals by soluble hydrogenase from Alcaligenes eutrophus H16. Biochem J 193(1):99-107
23. Elstner E, Heupel A, Vaklinova S (1970) On the oxidation of hydroxylamine in isolated chloroplasts and the possible role of a peroxidase from spinach leaves in the oxidation of ascorbate and glycolate. Z. Pflanzenphysiol 62:184-200
24. Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186(1):189-195
25. Denisov ET, Af anasev IB (2010) Oxidation and Antioxidants in Organic Chemistry and Biology (CRC, Boca Raton, FL)
26. Bielski BH, Cabelli DE, Arudi RL, Ross AB (1985) Reactivity of HO/O radicals in aqueous solution. J Phys Chem Ref Data 14:1041
27. Yankovskaya V, et al. (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299(5607):700-704
28. Hirst J (2013) Mitochondrial complex I. Annu Rev Biochem 82(1):551-575
29. Feder N (1970) A heme-peptide as an ultrastructural tracer. J Histochem Cytochem 18(12):911-913
30. Wikströ m M (2004) Cytochrome c oxidase years of the elusive proton pump. Biochim Biophys Acta 1655(1- 3):241-247
31. Solomon EI, Augustine AJ, Yoon J (2008) O2 reduction to H2O by the multicopper oxidases. Dalton Trans (30):3921-3932
32. Moore AL, et al. (2013) Unraveling the heater: New insights into the structure of the alternative oxidase. Annu Rev Plant Biol 64(1):637-663
33. Sawers RG, Boxer DH (1986) Purification and properties of membrane-bound hydrogenase isoenzyme from anaerobic ally grown Escherichia coli K12. Eur J Biochem 156(2):265-275
34. Menon NK, Robbins J, Wendt JC, Shanmugam KT, Przybyla AE (1991) Mutational analysis and characterization of the Escheri chia coli hya operon, which encodes [NiFe] hydrogenase 1. J Bacteriol 173(15):4851-4861
35. Sø balle B, Poole RK (1999) Microbial ubiquinones: Multiple roles in respiration, gene regulation and oxidative stress management. Microbiology 145(Pt 8):1817-1830
36. Sawers RG, Ballantine SP, Boxer DH (1985) Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: Evi dence for a third isoenzyme. J Bacteriol 164(3): 1324-1331
37. Richard DJ, Sawers G, Sargent F, McWalter L, Boxer DH (1999) Transcriptional regulation in response to oxygen and nitrate of the operons encoding the [NiFe] hydrogenases 1 and 2 of Escherichia coli. Microbiology 145(Pt 10):2903-2912
38. Giel JL, Rodionov D, Liu M, Blattner FR, Kiley PJ (2006) IscR-dependent gene exp ression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol Microbiol 60(4):1058-1075
39. Atlung T, Knudsen K, Heerfordt L, Brøndsted L (1997) Effects of sigmaS and the transcriptional activator AppY on induction of the Escherichia coli hya and cbdABappA operons in response to carbon and phosphate starvation. J Bacteriol 179(7): 2141-2146
40. Nitschke W, Russell MJ (2009) 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(5):481-496
41. S leep NH, Bird DK (2008) Evolutionary ecology during the rise of dioxygen in the Earth?s atmosphere. Philos Trans R Soc Lond B Biol Sci 363(1504):2651-2664
42. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25(4):455-501
43. Chance B (1957) Techniques for the assay of the respiratory enzymes. Methods in Enzymology (Academic, New York), Vol 4, pp 273-329
44. Nelson ST (2000) A simple, practical methodology for routine VSMOW/SLAP normalization of water samples analyzed by continuous flow methods. Rapid Commun Mass Spectrom 14(12):1044-1046
45. Carepo M, et al. (2002) 17O ENDOR detection of a solvent-derived Ni-(OH(x))-Fe bridge that is lost upon activation of the hydrogenase from Desulfovibrio gigas. J Am Chem Soc 124(2):281-286
46. van der Zwaan JW, Coremans JMCC, Bouwens ECM, Albracht SPJ (1990) Effect of 17O2 and 13CO on EPR espectra of nickel in hydrogenase from Chromatium vinosum. Biochim Biophys Acta 1041(2):101-110