Proton transfer in the quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus during reduction of oxygen

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 10, 2012, Pages 1914-1920

  Salomonsson, Lina ^a   Reimann, Joachim ^a,c   Tosha, Takehiko ^b   Krause, Nils ^a,d   Gonska, Nathalie ^a   Shiro, Yoshitsugu ^b   Ädelroth, Pia ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b RIKEN SPring 8 Center   (Japan)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Carbon monoxide; Flow flash; Heme copper oxidase; Non heme iron; Proton transfer pathway

Indexed keywords

CARBON DIOXIDE; HEME; NITRIC OXIDE REDUCTASE; OXYGEN; QUINOL DEPENDENT NITRIC OXIDE REDUCTASE; UNCLASSIFIED DRUG;

CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVE SITE; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; PARACOCCUS DENITRIFICANS; PH; PRIORITY JOURNAL; PROTON TRANSPORT; REDUCTION; SPECTRUM; STEADY STATE; TURNOVER TIME;

BACTERIAL PROTEINS; GEOBACILLUS STEAROTHERMOPHILUS; HYDROQUINONES; ION TRANSPORT; OXIDOREDUCTASES; OXYGEN; PARACOCCUS DENITRIFICANS; PROTONS;

BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS; PARACOCCUS DENITRIFICANS;

EID: 84864688816     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.04.007     Document Type: Conference Paper

References (55)

1. P. Tavares, A.S. Pereira, J.J. Moura, and I. Moura Metalloenzymes of the denitrification pathway J. Inorg. Biochem. 100 2006 2087 2100
2. W.G. Zumft Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type J. Inorg. Biochem. 99 2005 194 215
3. N.J. Watmough, G. Butland, M.R. Cheesman, J.W. Moir, D.J. Richardson, and S. Spiro Nitric oxide in bacteria: synthesis and consumption Biochim. Biophys. Acta 1411 1999 456 474
4. T. Hino, S. Nagano, H. Sugimoto, T. Tosha, and Y. Shiro Molecular structure and function of bacterial nitric oxide reductase Biochim. Biophys. Acta 1817 2012 680 687
5. M. Saraste, and J. Castresana Cytochrome oxidase evolved by tinkering with denitrification enzymes FEBS Lett. 341 1994 1 4
6. J. van der Oost, A.P. de Boer, J.W. de Gier, W.G. Zumft, A.H. Stouthamer, and R.J. van Spanning The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase FEMS Microbiol. Lett. 121 1994 1 9
7. J. Hendriks, A. Warne, U. Gohlke, T. Haltia, C. Ludovici, M. Lübben, and M. Saraste The active site of the bacterial nitric oxide reductase is a dinuclear iron center Biochemistry 37 1998 13102 13109
8. P. Girsch, and S. deVries Purification and initial kinetic and spectroscopic characterization of NO reductase from Paracoccus denitrificans Biochim. Biophys. Acta 1318 1997 202 216
9. T. Hino, Y. Matsumoto, S. Nagano, H. Sugimoto, Y. Fukumori, T. Murata, S. Iwata, and Y. Shiro Structural basis of biological N2O generation by bacterial nitric oxide reductase Science 330 2010 1666 1670
10. M.M. Pereira, M. Santana, and M. Teixeira A novel scenario for the evolution of haem-copper oxygen reductases Biochim. Biophys. Acta 1505 2001 185 208
11. J. Hemp, and R.B. Gennis Diversity of the heme-copper superfamily in archaea: insights from genomics and structural modeling Results Probl. Cell Differ. 45 2008 1 31
12. F.L. Sousa, R.J. Alves, J.B. Pereira-Leal, M. Teixeira, and M.M. Pereira A bioinformatics classifier and database for heme-copper oxygen reductases PLoS One 6 2011 e19117
13. B. Heiss, K. Frunzke, and W.G. Zumft Formation of the N-N bond from nitric oxide by a membrane-bound cytochrome bc complex of nitrate-respiring (denitrifying) Pseudomonas stutzeri J. Bacteriol. 171 1989 3288 3297
14. F.H. Thorndycroft, G. Butland, D.J. Richardson, and N.J. Watmough A new assay for nitric oxide reductase reveals two conserved glutamate residues form the entrance to a proton-conducting channel in the bacterial enzyme Biochem. J. 401 2007 111 119
15. R. Cramm, A. Pohlmann, and B. Friedrich Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16 FEBS Lett. 460 1999 6 10
16. S. de Vries, M.J.F. Strampraad, S. Lu, P. Moënne-Loccoz, and I. Schröder Purification and characterization of the MQH(2): NO oxidoreductase from the hyperthermophilic archaeon Pyrobaculum aerophilum J. Biol. Chem. 278 2003 35861 35868
17. P. Brzezinski, and P. Ädelroth Design principles of proton-pumping haem-copper oxidases Curr. Opin. Struct. Biol. 16 2006 465 472
18. S. Yoshikawa, K. Muramoto, and K. Shinzawa-Itoh Proton-pumping mechanism of cytochrome C oxidase Annu. Rev. Biophys. 40 2011 205 223
19. M.M. Pereira, F.L. Sousa, A.F. Verissimo, and M. Teixeira Looking for the minimum common denominator in haem-copper oxygen reductases: towards a unified catalytic mechanism Biochim. Biophys. Acta 1777 2008 929 934
20. V.R. Kaila, M.I. Verkhovsky, and M. Wikström Proton-coupled electron transfer in cytochrome oxidase Chem. Rev. 110 2010 7062 7081
21. H. Han, J. Hemp, L.A. Pace, H. Ouyang, K. Ganesan, J.H. Roh, F. Daldal, S.R. Blanke, and R.B. Gennis Adaptation of aerobic respiration to low O2 environments Proc. Natl. Acad. Sci. U.S.A. 108 2011 14109 14114
22. H.J. Lee, J. Reimann, Y. Huang, and P. Ädelroth Functional proton transfer pathways in the heme-copper oxidase superfamily Biochim. Biophys. Acta 1817 2012 537 544
23. P. Brzezinski, and P. Ädelroth Pathways of proton transfer in cytochrome c oxidase J. Bioenerg. Biomembr. 30 1998 99 107
24. M. Wikström, A. Jasaitis, C. Backgren, A. Puustinen, and M.I. Verkhovsky The role of the D- and K-pathways of proton transfer in the function of the haem-copper oxidases Biochim. Biophys. Acta 1459 2000 514 520
25. G. Butland, S. Spiro, N.J. Watmough, and D.J. Richardson Two conserved glutamates in the bacterial nitric oxide reductase are essential for activity but not assembly of the enzyme J. Bacteriol. 183 2001 189 199
26. D.H. Kastrau, B. Heiss, P.M. Kroneck, and W.G. Zumft Nitric oxide reductase from Pseudomonas stutzeri, a novel cytochrome bc complex. Phospholipid requirement, electron paramagnetic resonance and redox properties Eur. J. Biochem. 222 1994 293 303
27. H. Kumita, K. Matsuura, T. Hino, S. Takahashi, H. Hori, Y. Fukumori, I. Morishima, and Y. Shiro NO reduction by nitric-oxide reductase from denitrifying bacterium Pseudomonas aeruginosa: characterization of reaction intermediates that appear in the single turnover cycle J. Biol. Chem. 279 2004 55247 55254
28. J.P. Shapleigh, and W.J. Payne Nitric oxide-dependent proton translocation in various denitrifiers J. Bacteriol. 163 1985 837 840
29. J.H. Hendriks, A. Jasaitis, M. Saraste, and M.I. Verkhovsky Proton and electron pathways in the bacterial nitric oxide reductase Biochemistry 41 2002 2331 2340
30. J. Reimann, U. Flock, H. Lepp, A. Honigmann, and P. Ädelroth A pathway for protons in nitric oxide reductase from Paracoccus denitrificans Biochim. Biophys. Acta 1767 2007 362 373
31. K.R. Barth, V.M. Isabella, and V.L. Clark Biochemical and genomic analysis of the denitrification pathway within the genus Neisseria Microbiology 155 2009 4093 4103
32. Y. Matsumoto, T. Tosha, A.V. Pisliakov, T. Hino, H. Sugimoto, S. Nagano, Y. Sugita, and Y. Shiro Crystal structure of quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus Nat. Struct. Mol. Biol. 19 2012 238 246
33. S. Buschmann, E. Warkentin, H. Xie, J.D. Langer, U. Ermler, and H. Michel The structure of cbb3 cytochrome oxidase provides insights into proton pumping Science 329 2010 327 330
34. S. Iwata, C. Ostermeier, B. Ludwig, and H. Michel Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans Nature 376 1995 660 669
35. T. Soulimane, G. Buse, G.P. Bourenkov, H.D. Bartunik, R. Huber, and M.E. Than Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus EMBO J. 19 2000 1766 1776
36. T. Tsukihara, H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å Science 272 1996 1136 1144
37. U. Flock, N.J. Watmough, and P. Ädelroth Electron/proton coupling in bacterial nitric oxide reductase during reduction of oxygen Biochemistry 44 2005 10711 10719
38. T. Fujiwara, and Y. Fukumori Cytochrome cb-type nitric oxide reductase with cytochrome c oxidase activity from Paracoccus denitrificans Atcc 35512 J. Bacteriol. 178 1996 1866 1871
39. N. Sakurai, and T. Sakurai Isolation and characterization of nitric oxide reductase from Paracoccus halodenitrificans Biochemistry 36 1997 13809 13815
40. Q.H. Gibson, and C. Greenwood Reactions of cytochrome oxidase with oxygen and carbon monoxide Biochem. J. 86 1963 541 554
41. D.A. Proshlyakov, M.A. Pressler, and G.T. Babcock Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 95 1998 8020 8025
42. M.I. Verkhovsky, J.E. Morgan, M.L. Verkhovskaya, and M. Wikström Translocation of electrical charge during a single turnover of cytochrome-c oxidase Biochim. Biophys. Acta 1318 1997 6 10
43. I. Smirnova, J. Reimann, C. von Ballmoos, H.Y. Chang, R.B. Gennis, J.A. Fee, P. Brzezinski, and P. Ädelroth Functional role of Thr-312 and Thr-315 in the proton-transfer pathway in ba3 Cytochrome c oxidase from Thermus thermophilus Biochemistry 49 2010 7033 7039
44. Y. Huang, J. Reimann, H. Lepp, N. Drici, and P. Ädelroth Vectorial proton transfer coupled to reduction of O2 and NO by a heme-copper oxidase Proc. Natl. Acad. Sci. U.S.A. 105 2008 20257 20262
45. P. Lachmann, Y. Huang, J. Reimann, U. Flock, and P. Ädelroth Substrate control of internal electron transfer in bacterial nitric-oxide reductase J. Biol. Chem. 285 2010 25531 25537
46. E. Pinakoulaki, S. Gemeinhardt, M. Saraste, and C. Varotsis Nitric-oxide reductase. Structure and properties of the catalytic site from resonance Raman scattering J. Biol. Chem. 277 2002 23407 23413
47. U. Flock, P. Lachmann, J. Reimann, N.J. Watmough, and P. Ädelroth Exploring the terminal region of the proton pathway in the bacterial nitric oxide reductase J. Inorg. Biochem. 103 2009 845 850
48. U. Flock, F.H. Thorndycroft, A.D. Matorin, D.J. Richardson, N.J. Watmough, and P. Ädelroth Defining the proton entry point in the bacterial respiratory nitric-oxide reductase J. Biol. Chem. 283 2008 3839 3845
49. M. Brändén, H. Sigurdson, A. Namslauer, R.B. Gennis, P. Ädelroth, and P. Brzezinski On the role of the K-proton transfer pathway in cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 98 2001 5013 5018
50. J.H. Hendriks, L. Prior, A.R. Baker, A.J. Thomson, M. Saraste, and N.J. Watmough Reaction of carbon monoxide with the reduced active site of bacterial nitric oxide reductase Biochemistry 40 2001 13361 13369
51. L.C. Bell, D.J. Richardson, and S.J. Ferguson Identification of nitric oxide reductase activity in Rhodobacter capsulatus: the electron transport pathway can either use or bypass both cytochrome c2 and the cytochrome bc1 complex J. Gen. Microbiol. 138 1992 437 443
52. L.M. Blomberg, M.R. Blomberg, and P.E. Siegbahn A theoretical study on nitric oxide reductase activity in a ba(3)-type heme-copper oxidase Biochim. Biophys. Acta 1757 2006 31 46
53. M.I. Verkhovsky, J.E. Morgan, and M. Wikström Redox transitions between oxygen intermediates in cytochrome-c oxidase Proc. Natl. Acad. Sci. U.S.A. 93 1996 12235 12239
54. M. Karpefors, P. Ädelroth, Y. Zhen, S. Ferguson-Miller, and P. Brzezinski Proton uptake controls electron transfer in cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 95 1998 13606 13611
55. E.A. Gorbikova, M. Wikström, and M.I. Verkhovsky The protonation state of the cross-linked tyrosine during the catalytic cycle of cytochrome c oxidase J. Biol. Chem. 283 2008 34907 34912