Molecular mechanism of energy conservation in polysulfide respiration

Nature Structural and Molecular Biology

Volumn 15, Issue 7, 2008, Pages 730-737

  Jormakka, Mika ^a,b,c   Yokoyama, Ken ^d,e   Yano, Takahiro ^e   Tamakoshi, Masatada ^f   Akimoto, Satoru ^e   Shimamura, Tatsuro ^e,g   Curmi, Paul ^a   Iwata, So ^e,h,i  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b CENTENARY INSTITUTE   (Australia)

^c University of Sydney   (Australia)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^g Harima Institute ^*  (Japan)

^h IMPERIAL COLLEGE LONDON   (United Kingdom)

ⁱ RIKEN YOKOHAMA INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MENAQUINONE; MENAQUINONE 7; OXIDOREDUCTASE; POLYSULFIDE REDUCTASE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBUNIT; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY CHAIN; THERMUS THERMOPHILUS;

BINDING SITES; CATALYTIC DOMAIN; CELL MEMBRANE; DIMERIZATION; ELECTRON TRANSPORT; ELECTRONS; ELECTROSTATICS; ENERGY METABOLISM; MODELS, MOLECULAR; OXIDOREDUCTASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; PROTONS; QUINONES; SULFIDES; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

EID: 46449133263     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1434     Document Type: Article

References (59)

1. Henne, A. et al. The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 22, 547-553 (2004).
2. Yano, T., Chu, S.S., Sled', V.D., Ohnishi, T. & Yagi, T. The proton-translocating NADH-quinone oxidoreductase (NDH-1) of thermophilic bacterium Thermus thermophilus HB-8. Complete DNA sequence of the gene cluster and thermostable properties of the expressed NQO2 subunit. J. Biol. Chem. 272, 4201-4211 (1997).
3. Collins, M.D., Shah, H.N. & Minnikin, D.E. A note on the separation of natural mixtures of bacterial menaquinones using reverse phase thin-layer chromatography. J. Appl. Bacteriol. 48, 277-282 (1980).
4. 552 from an extreme thermophile, Thermus thermophilus HB8. J. Biochem. 82, 769-776 (1977).
5. 1 complex complements the respiratory chain of Thermus thermophilus. Biochim. Biophys. Acta 1708, 262-274 (2005).
6. 3: a second terminal oxidase from the extreme thermophile Thermus thermophilus. Proc. Natl. Acad. Sci. USA 85, 5779-5783 (1988).
7. 3 from the thermophilic bacterium Thermus thermophilus: a member of the heme-copper oxidase superfamily. J. Bioenerg. Biomembr. 25, 103-114 (1993).
8. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19, 1766-1776 (2000).
9. 3 from Thermus thermophilus HB8. J. Biol. Chem. 270, 21016-21020 (1995).
10. Fee, J.A., Choc, M.G., Findling, K.L., Lorence, R. & Yoshida, T. Properties of a copper-containing cytochrome c1aa3 complex: a terminal oxidase of the extreme thermophile Thermus thermophilus HB8. Proc. Natl. Acad. Sci. USA 77, 147-151 (1980).
11. Brock, T.D. Thermophilic microorganisms and life at high temperatures. (Springer, New York, 1978).
12. Blöchl, E. et al. Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 °C. Extremophiles 1, 14-21 (1997).
13. Xu, Y., Schoonen, M.A.A., Nordstrom, D.K., Cunningham, K.M. & Ball, J.W. Sulfur geochemistry of hydrothermal waters in Yellowstone National Park, Wyoming, USA II. Formation and decomposition of thiosulfate and polythionate in Cinder Pool. J. Volcanol. Geotherm. Res. 97, 407-423 (2000).
14. Rothery, R.A., Workun, G.J. & Weiner, J.H. The prokaryotic complex iron-sulfur molybdoenzyme family. Biochim. Biophys. Acta published online, doi:10.1016/j.bbamem.2007.09.002 (18 September 2007).
15. Rothery, R.A., Kalra, N., Turner, R.J. & Weiner, J.H. Sequence similarity as a predictor of the transmembrane topology of membrane-intrinsic subunits of bacterial respiratory chain enzymes. J. Mol. Microbiol. Biotechnol. 4, 133-150 (2002).
16. Jormakka, M., Törnroth, S., Byrne, B. & Iwata, S. Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295, 1863-1868 (2002).
17. Bertero, M.G. et al. Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat. Struct. Biol. 10, 681-687 (2003).
18. Gavira, M., Roldán, M.D., Castillo, F. & Moreno-Vivián, C. Regulation of nap gene expression and periplasmic nitrate reductase activity in the phototrophic bacterium Rhodobacter sphaeroides DSM158. J. Bacteriol. 184, 1693-1702 (2002).
19. Ellington, M.J. et al. Characterization of the expression and activity of the periplasmic nitrate reductase of Paracoccus pantotrophus in chemostat cultures. Microbiology 149, 1533-1540 (2003).
20. Ansaldi, M., Théraulaz, L., Baraquet, C., Panis, G. & Méjean, V. Aerobic TMAO respiration in Escherichia coli. Mol. Microbiol. 66, 484-494 (2007).
21. Raaijmakers, H.C. & Romão, M.J. Formate-reduced E. coli formate dehydrogenase H: the reinterpretation of the crystal structure suggests a new reaction mechanism. J. Biol. Inorg. Chem. 11, 849-854 (2006).
22. McMaster, J. & Enemark, J.H. The active sites of molybdenum- and tungsten-containing enzymes. Curr. Opin. Chem. Biol. 2, 201-207 (1998).
23. Hille, R. The mononuclear molybdenum enzymes. Chem. Rev. 96, 2757-2816 (1996).
24. Weiner, J.H., Shaw, G., Turner, R.J. & Trieber, C.A. The topology of the anchor subunit of dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 268, 3238-3244 (1993).
25. Santini, C.L. et al. A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17, 101-112 (1998).
26. Schindelin, H., Kisker, C., Hilton, J., Rajagopalan, K.V. & Rees, D.C. Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination. Science 272, 1615-1621 (1996).
27. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
28. Simala-Grant, J.L. & Weiner, J.H. Modulation of the substrate specificity of Escherichia coli dimethylsulfoxide reductase. Eur. J. Biochem. 251, 510-515 (1998).
29. Berglund, G.I. et al. The catalytic pathway of horseradish peroxidase at high resolution. Nature 417, 463-468 (2002).
30. Matsui, T., Ozaki, S., Liong, E., Phillips, G.N. & Watanabe, Y. Effects of the location of distal histidine in the reaction of myoglobin with hydrogen peroxide. J. Biol. Chem. 274, 2838-2844 (1999).
31. Ridge, J.P., Aguey-Zinsou, K.F., Bernhardt, P.V., Hanson, G.R. & McEwan, A.G. The critical role of tryptophan-116 in the catalytic cycle of dimethylsulfoxide reductase from Rhodobacter capsulatus. FEBS Lett. 563, 197-202 (2004).
32. Hille, R. Molybdenum enzymes. Essays Biochem. 34, 125-137 (1999).
33. Hensel, M., Hinsley, A.P., Nikolaus, T., Sawers, G. & Berks, B.C. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol. Microbiol. 32, 275-287 (1999).
34. Nagarajan, K. et al. Structural and functional analogue of the active site of polysulfide reductase from Wolinella succinogenes. Inorg. Chem. 43, 4532-4533 (2004).
35. Berks, B.C. et al. Sequence analysis of subunits of the membrane-bound nitrate reductase from a denitrifying bacterium: the integral membrane subunit provides a prototype for the dihaem electron-carrying arm of a redox loop. Mol. Microbiol. 15, 319-331 (1995).
36. Page, C.C., Moser, C.C., Chen, X. & Dutton, P.L. Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature 402, 47-52 (1999).
37. Cheng, V.W., Rothery, R.A., Bertero, M.G., Strynadka, N.C. & Weiner, J.H. Investigation of the environment surrounding iron-sulfur cluster 4 of Escherichia coli dimethylsulfoxide reductase. Biochemistry 44, 8068-8077 (2005).
38. Dietrich, W. & Klimmek, O. The function of methyl-menaquinone-6 and polysulfide reductase membrane anchor (PsrC) in polysulfide respiration of Wolinella succinogenes. Eur. J. Biochem. 269, 1086-1095 (2002).
39. Szilágyi, A. & Závodszky, P. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8, 493-504 (2000).
40. Yankovskaya, V. et al. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299, 700-704 (2003).
41. Lancaster, C.R., Kröger, A., Auer, M. & Michel, H. Structure of fumarate reductase from Wolinella succinogenes at 2.2 Å resolution. Nature 402, 377-385 (1999).
42. Iverson, T.M., Luna-Chavez, C., Cecchini, G. & Rees, D.C. Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284, 1961-1966 (1999).
43. Sun, F. et al. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043-1057 (2005).
44. Huang, L.S. et al. 3-nitropropionic acid is a suicide inhibitor of mitochondrial respiration that, upon oxidation by complex II, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme. J. Biol. Chem. 281, 5965-5972 (2006).
45. Horsefield, R. et al. Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction. J. Biol. Chem. 281, 7309-7316 (2006).
46. Hedderich, R. et al. Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol. Rev. 22, 353-381 (1998).
47. Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. Structure at 2.8 resolution of cytochrome C oxidase from Paracoccus denitrificans. Nature 376, 660-669 (1995).
48. Tsukihara, T. et al. The whole structure of the 13-subunit oxidized cytochrome C oxidase at 2.8. Science 272, 1136-1144 (1996).
49. Holt, P.J., Morgan, D.J. & Sazanov, L.A. The location of NuoL and NuoM subunits in the membrane domain of the Escherichia coli complex I: implications for the mechanism of proton pumping. J. Biol. Chem. 278, 43114-43120 (2003).
50. Ohnishi, T. & Salerno, J.C. Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett. 579, 4555-4561 (2005).
51. - stoichiometry for NADH dehydrogenase I and dimethyl solfoxide reductase in anaerobically grown Escherichia coli cells. J. Bacteriol. 178, 6233-6237 (1996).
52. Yokoyama, K., Akabane, Y., Ishii, N. & Yoshida, M. Isolation of prokaryotic V0V1-ATPase from a thermophilic eubacterium Thermus thermophilus. J. Biol. Chem. 269, 12248-12253 (1994).
53. Otwinowski, Z. & Minor, W. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
54. Leslie, A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EAMCB Newsletter on Protein Crystallography, No. 26 (Daresbury Laboratory, Warrington, UK, 1992).
55. Collaborative Computational Project. Number 4. The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr. D50, 760-763 (1994).
56. Weeks, C.M. & Miller, R. The design and implementation of SnB v2.0. J. Appl. Crystallogr. 32, 120-124 (1999).
57. Perrakis, A., Morris, R.M. & Lamzin, V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6, 458-463 (1999).
58. Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
59. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).