A cytochrome c containing nitrate reductase plays a role in electron transport for denitrification in Thermus thermophilus without involvement of the bc respiratory complex

Molecular Microbiology

Volumn 70, Issue 2, 2008, Pages 507-518

  Cava, Felipe ^a   Zafra, Olga ^a   Berenguer, José ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; MUTANT PROTEIN; NITRATE; NITRATE REDUCTASE; NITRIC OXIDE; NITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANAEROBIC GROWTH; ARTICLE; CONTROLLED STUDY; DENITRIFICATION; ELECTRON TRANSPORT; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; THERMUS THERMOPHILUS;

ANAEROBIOSIS; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; CYTOCHROMES C; ELECTRON TRANSPORT; GENES, REPORTER; HEME; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; MUTATION; NAD; NITRATE REDUCTASE; NITRATES; NITRIC OXIDE; NITRITES; NITROGEN; OXIDATION-REDUCTION; THERMUS THERMOPHILUS;

THERMUS THERMOPHILUS;

EID: 52649114346     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06429.x     Document Type: Article

References (41)

1. Berks, B.C., Ferguson, S.J., Moir, J.W. Richardson, D.J. (1995) Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim Biophys Acta 1232 : 97 173.
2. Berry, E.A., Guergova-Kuras, M., Huang, L.S. Crofts, A.R. (2000) Structure and function of cytochrome bc complexes. Annu Rev Biochem 69 : 1005 1075.
3. Bertero, M.G., Rothery, R.A., Palak, M., Hou, C., Lim, D., Blasco, F., et al. (2003) Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat Struct Biol 10 : 681 687.
4. Brouns, S.J., Wu, H., Akerboom, J., Turnbull, A.P., de Vos, W.M. van der Oost, J. (2005) Engineering a selectable marker for hyperthermophiles. J Biol Chem 280 : 11422 11431.
5. Cava, F. Berenguer, J. (2006) Biochemical and regulatory properties of a respiratory island encoded by a conjugative plasmid in the extreme thermophile Thermus thermophilus. Biochem Soc Trans 34 : 97 100.
6. Cava, F., Zafra, O., Magalon, A., Blasco, F. Berenguer, J. (2004) A new type of NADH dehydrogenase specific for nitrate respiration in the extreme thermophile Thermus thermophilus. J Biol Chem 279 : 45369 45378.
7. Cava, F., Laptenko, O., Borukhov, S., Chahlafi, Z., Blas-Galindo, E., Gomez-Puertas, P. Berenguer, J. (2007) Control of the respiratory metabolism of Thermus thermophilus by the nitrate respiration conjugative element NCE. Mol Microbiol 64 : 630 646.
8. Cava, F., Zafra, O., da Costa, M.S. Berenguer, J. (2008a) The role of the nitrate respiration element of Thermus thermophilus in the control and activity of the denitrification apparatus. Environ Microbiol 10 : 522 533.
9. Cava, F., de Pedro, M.A., Blas-Galindo, E., Waldo, G.S., Westblade, L.F. Berenguer, J. (2008b) Expression and use of superfolder green fluorescent protein at high temperatures in vivo: a tool to study extreme thermophile biology. Environ Microbiol 10 : 605 613.
10. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166 : 557 580.
11. Hartmann, R.K., Wolters, B., Kroger, B., Shultze, S., Spetch, T. Erdmann, V.A. (1989) Does Thermus represent another deep eubacterial branching? Syst Appl Microbiol 11 : 243 249.
12. Karimova, G., Pidoux, J., Ullmann, A. Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95 : 5752 5756.
13. Karimova, G., Ullmann, A. Ladant, D. (2001) Protein-protein interaction between Bacillus stearothermophilus tyrosyl-tRNA synthetase subdomains revealed by a bacterial two-hybrid system. J Mol Microbiol Biotechnol 3 : 73 82.
14. Karimova, G., Ladant, D. Ullmann, A. (2002) Two-hybrid systems and their usage in infection biology. Int J Med Microbiol 292 : 17 25.
15. Koyama, Y., Hoshino, T., Tomizuka, N. Furukawa, K. (1986) Genetic transformation of the extreme thermophile Thermus thermophilus and of other Thermus spp. J Bacteriol 166 : 338 340.
16. Lasa, I., Castón, J.R., Fernandez-Herrero, L.A., Pedro, M.A. Berenguer, J. (1992) Insertional mutagenesis in the extreme thermophilic eubacteria Thermus thermophilus. Mol Microbiol 11 : 1555 1564.
17. Lennox, E.S. (1955) Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1 : 190 206.
18. Manaia, C.M., Hoste, B., Gutierrez, M.C., Gillis, M., Ventosa, A., Kersters, K. da Costa, M.S. (1994) Halotolerant Thermus strains from marine and terrestrial hot springs belong to Thermus thermophilus (ex Oshima and Imahori, 1974) nom. rev. emend. Syst Appl Microbiol 17 : 526 532.
19. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia Coli and Related Bacteria. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
20. Mooser, D., Maneg, O., Corvey, C., Steiner, T., Malatesta, F., Karas, M., et al. (2005) A four-subunit cytochrome bc (1) complex complements the respiratory chain of Thermus thermophilus. Biochim Biophys Acta 1708 : 262 274.
21. Mooser, D., Maneg, O., MacMillan, F., Malatesta, F., Soulimane, T. Ludwig, B. (2006) The menaquinol-oxidizing cytochrome bc complex from Thermus thermophilus: protein domains and subunits. Biochim Biophys Acta 1757 : 1084 1095.
22. Moreno, R., Zafra, O., Cava, F. Berenguer, J. (2003) Development of a gene expression vector for Thermus thermophilus based on the promoter of the respiratory nitrate reductase. Plasmid 49 : 2 8.
23. Nakamura, A., Takakura, Y., Kobayashi, H. Hoshino, T. (2005) In vivo directed evolution for thermostabilization of Escherichia coli hygromycin B phosphotransferase and the use of the gene as a selection marker in the host-vector system of Thermus thermophilus. J Biosci Bioeng 100 : 158 163.
24. Pereira, M.M., Bandeiras, T.M., Fernandes, A.S., Lemos, R.S., Melo, A.M. Teixeira, M. (2004) Respiratory chains from aerobic thermophilic prokaryotes. J Bioenerg Biomembr 36 : 93 105.
25. Ramirez-Arcos, S., Fernandez-Herrero, L.A., Marin, I. Berenguer, J. (1998a) Anaerobic growth, a property horizontally transferred by an Hfr-like mechanism among extreme thermophiles. J Bacteriol 180 : 3137 3143.
26. Ramirez-Arcos, S., Fernandez-Herrero, L.A. Berenguer, J. (1998b) A thermophilic nitrate reductase is responsible for the strain specific anaerobic growth of Thermus thermophilus HB8. Biochim Biophys Acta 1396 : 215 227.
27. Richardson, D.J. (2000) Bacterial respiration: a flexible process for a changing environment. Microbiology 146 : 551 571.
28. Richardson, D.J., Berks, B.C., Russell, D.A., Spiro, S. Taylor, C.J. (2001) Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58 : 165 178.
29. Sambrook, J., Fritsch, E. Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual. New York : Cold Spring Harbor Laboratory Press.
30. Sazanov, L.A. Hinchliffe, P. (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 : 1430 1436.
31. Schutz, M., Brugna, M., Lebrun, E., Baymann, F., Huber, R., Stetter, K.O., et al. (2000) Early evolution of cytochrome bc complexes. J Mol Biol 300 : 663 675.
32. Snell, F.D. Snell, C.T. (1949) Colorimetric Methods of Analysis. New York : Van Nostrand.
33. Soulimane, T., von Walter, M., Hof, P., Than, M.E., Huber, R. Buse, G. (1997) Cytochrome-c552 from Thermus thermophilus: a functional and crystallographic investigation. Biochem Biophys Res Commun 237 : 572 576.
34. Soulimane, T., Buse, G., Bourenkov, G.P., Bartunik, H.D., Huber, R. Than, M.E. (2000) Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus. EMBO J 19 : 1766 1776.
35. Stroh, A., Anderka, O., Pfeiffer, K., Yagi, T., Finel, M., Ludwig, B. Schagger, H. (2004) Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J Biol Chem 279 : 5000 5007.
36. Tavares, P., Pereira, A.S., Moura, J.J. Moura, I. (2006) Metalloenzymes of the denitrification pathway. J Inorg Biochem 100 : 2087 2100.
37. 552: a new highly thermostable cytochrome-c structure obtained by MAD phasing. J Mol Biol 271 : 629 644.
38. Yagi, T., Hon-nami, K. Ohnishi, T. (1988) Purification and characterization of two types of NADH-quinone reductase from Thermus thermophilus HB-8. Biochemistry 27 : 2008 2013.
39. Zafra, O., Ramirez, S., Castan, P., Moreno, R., Cava, F., Valles, C., et al. (2002) A cytochrome c encoded by the nar operon is required for the synthesis of active respiratory nitrate reductase in Thermus thermophilus. FEBS Lett 523 : 99 102.
40. Zafra, O., Cava, F., Blasco, F., Magalon, A. Berenguer, J. (2005) Membrane-associated maturation of the heterotetrameric nitrate reductase of Thermus thermophilus. J Bacteriol 187 : 3990 3996.
41. Zumft, W.G. (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61 : 533 616.