Rapid Electron Transfer within the III-IV Supercomplex in Corynebacterium glutamicum

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Graf, Simone ^a,b   Fedotovskaya, Olga ^a   Kao, Wei Chun ^c   Hunte, Carola ^c   Ädelroth, Pia ^a   Bott, Michael ^d   Von Ballmoos, Christoph ^b   Brzezinski, Peter ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF FREIBURG   (Germany)

^d FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84989229016     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep34098     Document Type: Article

References (61)

1. Schägger, H. Respiratory chain supercomplexes. IUBMB Life 52, 119-128 (2002).
2. Stuart, R. A. Supercomplex organization of the oxidative phosphorylation enzymes in yeast mitochondria. J. Bioenerg. Biomembr. 40, 411-417 (2008).
3. Heinemeyer, J., Braun, H. P., Boekema, E. J., Kouil, R. A structural model of the cytochrome c reductase/oxidase supercomplex from yeast mitochondria. J. Biol. Chem. 282, 12240-12248 (2007).
4. Winge, D. R. Sealing the Mitochondrial Respirasome. Molecular and Cellular Biology 32, 2647-2652 (2012).
5. Mileykovskaya, E. et al. Arrangement of the respiratory chain complexes in Saccharomyces cerevisiae supercomplex III2IV2 revealed by single particle cryo-electron microscopy. J. Biol. Chem. 287, 23095-23103, doi: 10.1074/jbc.M112.367888 (2012).
6. Genova, M. L., Lenaz, G. Functional role of mitochondrial respiratory supercomplexes. Biochimica et Biophysica Acta-Bioenergetics 1837, 427-443, doi: 10.1016/j.bbabio.2013.11.002 (2014).
7. Acin-Perez, R., Enriquez, J. A. The function of the respiratory supercomplexes: The plasticity model. Biochimica et Biophysica Acta-Bioenergetics 1837, 444-450, doi: 10.1016/j.bbabio.2013.12.009 (2014).
8. Boumans, H., Grivell, L. A., Berden, J. A. The respiratory chain in yeast behaves as a single functional unit. J. Biol. Chem. 273, 4872-4877, doi: 10.1074/jbc.273.9.4872 (1998).
9. Althoff, T., Mills, D. J., Popot, J. L., Kühlbrandt, W. Arrangement of electron transport chain components in bovine mitochondrial supercomplex I 1 III 2 IV 1. EMBO Journal 30, 4652-4664, doi: 10.1038/emboj.2011.324 (2011).
10. Dudkina, N. V., Folea, I. M., Boekema, E. J. Towards structural and functional characterization of photosynthetic and mitochondrial supercomplexes. Micron 72, 39-51, doi: 10.1016/j.micron.2015.03.002 (2015).
11. Cruciat, C. M., Brunner, S., Baumann, F., Neupert, W., Stuart, R. A. The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 275, 18093-18098, doi: 10.1074/jbc.M001901200 (2000).
12. Berry, E. A., Trumpower, B. L. Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc1 and cytochrome c-aa3 complexes. J. Biol. Chem. 260, 2458-2467 (1985).
13. Sone, N., Sekimachi, M., Kutoh, E. Identification and properties of a quinol oxidase super-complex composed of a bc1 complex and cytochrome oxidase in the thermophilic bacterium PS3. J. Biol. Chem. 262, 15386-15391 (1987).
14. Stroh, A. et al. Assembly of Respiratory Complexes I, III, and IV into NADH Oxidase Supercomplex Stabilizes Complex I in Paracoccus denitrificans. J. Biol. Chem. 279, 5000-5007, doi: 10.1074/jbc.M309505200 (2004).
15. Reincke, B. et al. Heterologous expression of soluble fragments of cytochrome c552 acting as electron donor to the Paracoccus denitrificans cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1411, 114-120, doi: 10.1016/s0005-2728(99)00037-7 (1999).
16. Myllykallio, H., Drepper, F., Mathis, P., Daldal, F. Membrane-anchored cytochrome c(y) mediated microsecond time range electron transfer from the cytochrome bc1 complex to the reaction center in Rhodobacter capsulatus. Biochemistry 37, 5501-5510, doi: 10.1021/bi973123d (1998).
17. Daldal, F. et al. Mobile cytochrome c2 and membrane-anchored cytochrome cy are both efficient electron donors to the cbb3-and aa3-type cytochrome c oxidases during respiratory growth of Rhodobacter sphaeroides. J. Bacteriol. 183, 2013-2024, doi: 10.1128/jb.183.6.2013-2024.2001 (2001).
18. Sakamoto, J. et al. Cytochrome c oxidase contains an extra charged amino acid cluster in a new type of respiratory chain in the amino-acid-producing Gram-positive bacterium Corynebacterium glutamicum. Microbiology 147, 2865-2871 (2001).
19. Bott, M., Niebisch, A. The respiratory chain of Corynebacterium glutamicum. Journal of Biotechnology 104, 129-153, doi: 10.1016/s0168-1656(03)00144-5 (2003).
20. Niebisch, A., Bott, M. Purification of a cytochrome bc1-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum: Identification of a fourth subunit of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1. J. Biol. Chem. 278, 4339-4346, doi: 10.1074/jbc.M210499200 (2003).
21. Niebisch, A., Bott, M. Molecular analysis of the cytochrome bc1-aa3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c1. Archives of Microbiology 175, 282-294, doi: 10.1007/s002030100262 (2001).
22. Sone, N. et al. A novel hydrophobic diheme c-type cytochrome. Purification from Corynebacterium glutamicum and analysis of the QcrCBA operon encoding three subunit proteins of a putative cytochrome reductase complex. Biochimica et Biophysica Acta-Bioenergetics 1503, 279-290, doi: 10.1016/s0005-2728(00)00205-x (2001).
23. Kao, W.-C. et al. The obligate respiratory supercomplex from Actinobacteria. Biochimica et Biophysica Acta (BBA)-Bioenergetics, http://dx.doi.org/10.1016/j.bbabio.2016.07.009.
24. Megehee, J. A., Hosler, J. P., Lundrigan, M. D. Evidence for a cytochrome bcc-aa3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology 152, 823-829, doi: 10.1099/mic.0.28723-0 (2006).
25. Hunte, C., Koepke, J., Lange, C., Roßmanith, T., Michel, H. Structure at 2.3 A resolution of the cytochrome bc1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure 8, 669-684, doi: 10.1016/S0969-2126(00)00152-0 (2000).
26. Hemp, J., Gennis, R. B. Diversity of the heme-copper superfamily in archaea: insights from genomics and structural modeling. Results Probl Cell Differ 45, 1-31 (2008).
27. Pereira, M. M., Santana, M., Teixeira, M. A novel scenario for the evolution of haem-copper oxygen reductases. Biochim. Biophys. Acta-Bioenerg. 1505, 185-208 (2001).
28. Hosler, J. P., Ferguson-Miller, S., Mills, D. A. Energy transduction: Proton transfer through the respiratory complexes. Annual Review of Biochemistry 75, 165-187 (2006).
29. Yoshikawa, S. et al. Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1757, 1110-1116 (2006).
30. Namslauer, A., Brzezinski, P. Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett 567, 103-110 (2004).
31. Brzezinski, P., Gennis, R. B. Cytochrome c oxidase: exciting progress and remaining mysteries. J. Bioenerg. Biomembr. 40, 521-531 (2008).
32. Brzezinski, P., Ädelroth, P. Design principles of proton-pumping haem-copper oxidases. Curr Opin Struct Biol 16, 465-472 (2006).
33. Richter, O. M. H., Ludwig, B. Electron transfer and energy transduction in the terminal part of the respiratory chain-Lessons from bacterial model systems. Biochimica et Biophysica Acta-Bioenergetics 1787, 626-634 (2009).
34. Belevich, I., Verkhovsky, M. I. Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid Redox Signal 10, 1-29 (2008).
35. Ferguson-Miller, S., Hiser, C., Liu, J. Gating and regulation of the cytochrome c oxidase proton pump. Biochimica et Biophysica Acta-Bioenergetics 1817, 489-494 (2012).
36. Rich, P. R., Maréchal, A. Functions of the hydrophilic channels in protonmotive cytochrome c oxidase. Journal of the Royal Society Interface 10, 183-196 (2013).
37. Kaila, V. R. I., Verkhovsky, M. I., Wikström, M. Proton-coupled electron transfer in cytochrome oxidase. Chem. Rev. 110, 7062-7081 (2010).
38. Ädelroth, P., Ek, M., Brzezinski, P. Factors Determining Electron-Transfer Rates in Cytochrome c Oxidase: Investigation of the Oxygen Reaction in the R. sphaeroides and Bovine Enzymes. Biochim. Biophys. Acta 1367, 107-117 (1998).
39. Svensson-Ek, M. et al. The X-ray Crystal Structures of Wild-Type and EQ(I-286) Mutant Cytochrome c Oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321, 329-339 (2002).
40. Biasini, M. et al. SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research 42, W252-W258, doi: 10.1093/nar/gku340 (2014).
41. Arnold, K., Bordoli, L., Kopp, J., Schwede, T. The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201, doi: 10.1093/bioinformatics/bti770 (2006).
42. Guex, N., Peitsch, M. C., Schwede, T. Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective. Electrophoresis 30, S162-S173, doi: 10.1002/elps.200900140 (2009).
43. Vanneste, W. H. The stoichiometry and absorption spectra of components a and a-3 in cytochrome c oxidase. Biochemistry 5, 838-848 (1966).
44. van Gelder, B. F. On cytochrome c oxidase. I. The extinction coefficients of cytochrome a and cytochrome a3. Biochimica Et Biophysica Acta 118, 36-46 (1966).
45. Michel, B., Bosshard, H. R. Spectroscopic analysis of the interaction between cytochrome c and cytochrome c oxidase. J. Biol. Chem. 259, 10085-10091 (1984).
46. Brzezinski, P., Johansson, A. L. Variable proton-pumping stoichiometry in structural variants of cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1797, 710-723 (2010).
47. Von Ballmoos, C., Gennis, R. B., Ädelroth, P., Brzezinski, P. Kinetic design of the respiratory oxidases. Proc. Natl. Acad. Sci. USA 108, 11057-11062 (2011).
48. Muntyan, M. S. et al. Cytochrome cbb3 of Thioalkalivibrio is a Na+ pumping cytochrome oxidase. Proc. Natl. Acad. Sci. USA 112, 7695-7700, doi: 10.1073/pnas.1417071112 (2015).
49. Park, C., Moon, J. Y., Cokic, P., Webster, D. A. Na+ translocating cytochrome bo terminal oxidase from Vitreoscilla: Some parameters of its Na+ pumping and orientation in synthetic vesicles. Biochemistry 35, 11895-11900, doi: 10.1021/bi9530503 (1996).
50. Einarsdóttir, Ó. et al. Photodissociation and recombination of carbonmonoxy cytochrome oxidase: dynamics from picoseconds to kiloseconds. Biochemistry 32, 12013-12024 (1993).
51. Karpefors, M., Ädelroth, P., Zhen, Y., Ferguson-Miller, S., Brzezinski, P. Proton uptake controls electron transfer in cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 95, 13606-13611 (1998).
52. Wang, K. F. et al. Definition of the interaction domain for cytochrome c on cytochrome c oxidase-II. Rapid kinetic analysis of electron transfer from cytochrome c to Rhodobacter sphaeroides cytochrome oxidase surface mutants. J. Biol. Chem. 274, 38042-38050 (1999).
53. Gray, H. B., Winkler, J. R. Long-range electron transfer. Proc. Natl. Acad. Sci. USA 102, 3534-3539, doi: 10.1073/pnas.0408029102 (2005).
54. Von Ballmoos, C. et al. Mutation of a single residue in the ba3 oxidase specifically impairs protonation of the pump site. Proc. Natl. Acad. Sci. USA 112, 3397-3402, doi: 10.1073/pnas.1422434112 (2015).
55. Vilhjálmsdóttir, J., Johansson, A. L., Brzezinski, P. Structural Changes and Proton Transfer in Cytochrome c Oxidase. Scientific Reports 5, doi: 10.1038/srep12047 (2015).
56. Salomonsson, L., Faxén, K., Ädelroth, P., Brzezinski, P. The timing of proton migration in membrane-reconstituted cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 102, 17624-17629 (2005).
57. Aagaard, A., Brzezinski, P. Zinc ions inhibit oxidation of cytochrome c oxidase by oxygen. FEBS Lett. 494, 157-160 (2001).
58. Namslauer, A., Aagaard, A., Katsonouri, A., Brzezinski, P. Intramolecular proton-transfer reactions in a membrane-bound proton pump: the effect of pH on the peroxy to ferryl transition in cytochrome c oxidase. Biochemsitry 42, 1488-1498 (2003).
59. Han, D. et al. Replacing Asn207 by Aspartate at the Neck of the D Channel in the aa3-Type Cytochrome c Oxidase from Rhodobacter sphaeroides Results in Decoupling the Proton Pump. Biochemistry 45, 14064-14074 (2006).
60. Namslauer, A., Pawate, A. S., Gennis, R. B., Brzezinski, P. Redox-coupled proton translocation in biological systems: Proton shuttling in cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 100, 15543-15547 (2003).
61. Kanzaki, T., Sugiyama, Y., Kitano, K., Ashida, Y., Imada, I. Quinones of brevibacterium. Biochimica et Biophysica Acta (BBA)/Lipids and Lipid Metabolism 348, 162-165, doi: 10.1016/0005-2760(74)90102-7 (1974).