Urocanate reductase: Identification of a novel anaerobic respiratory pathway in Shewanella oneidensis MR-1

Molecular Microbiology

Volumn 86, Issue 6, 2012, Pages 1452-1463

  Bogachev, Alexander V ^a   Bertsova, Yulia V ^a   Bloch, Dmitry A ^b   Verkhovsky, Michael I ^b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVOPROTEIN; HISTIDINE; UNCLASSIFIED DRUG; UROCANATE REDUCTASE; UROCANIC ACID;

ANAEROBIC GROWTH; ANAEROBIC RESPIRATION; ARTICLE; BACTERIAL SURVIVAL; BINDING AFFINITY; BIOCHEMISTRY; CLOSTRIDIUM TETANI; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FUSOBACTERIUM; GENE PRODUCT; GENETIC ANALYSIS; MICROBIAL RESPIRATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SHEWANELLA; SHEWANELLA ONEIDENSIS; TITRIMETRY;

ANAEROBIOSIS; CLONING, MOLECULAR; GENE EXPRESSION; KINETICS; METABOLIC NETWORKS AND PATHWAYS; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SHEWANELLA; SUBSTRATE SPECIFICITY; TRANSCRIPTIONAL ACTIVATION; UROCANIC ACID;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM; CLOSTRIDIUM TETANI; FUSOBACTERIUM; SHEWANELLA; SHEWANELLA ONEIDENSIS MR-1;

EID: 84871021131     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12067     Document Type: Article

References (50)

1. Alexeyev, M.F. (1999) The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques 26: 824-828.
2. Arkhipova, O.V., and Akimenko, V.K. (2005) Unsaturated organic acids as terminal electron acceptors for reductase chains of anaerobic bacteria. Microbiology 74: 629-639.
3. Backiel, J., Juárez, O., Zagorevski, D.V., Wang, Z., Nilges, M.J., and Barquera, B. (2008) Covalent binding of flavins to RnfG and RnfD in the Rnf complex from Vibrio cholerae. Biochemistry 47: 11273-11284.
4. + pump from Vibrio cholerae with covalently attached FMN. FEBS Lett 492: 45-49.
5. +-translocating NADH:quinone oxidoreductase from Vibrio cholerae. Biochemistry 41: 3781-3789.
6. Bender, R.A. (2012) Regulation of the histidine utilization (hut) system in bacteria. Microbiol Mol Biol Rev 76: 565-584.
7. +-translocating NADH:quinone oxidoreductase. Biochemistry 45: 3421-3428.
8. +-translocating NADH:quinone oxidoreductase. 2. Study of the enzyme by optical spectroscopy. Biochemistry 48: 6299-6304.
9. +-translocating NADH:quinone oxidoreductase from Vibrio cholerae. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 1677-1679.
10. Claverie, J.M. (2005) Fewer genes, more noncoding RNA. Science 309: 1529-1530.
11. 3+ by Shewanella frigidimarina NCIMB400. Biochem J 342: 439-448.
12. Ells, A.H. (1959) A colorimetric method for the assay of soluble succinic dehydogenase and pyridinenucleotide-linked dehydrogenases. Arch Biochem Biophys 85: 561-562.
13. Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.-y., et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics 15: 5.6.1-5.6.30.
14. +-translocating NADH:quinone oxidoreductase. Biochemistry (Mosc) 73: 123-129.
15. Gao, H., Barua, S., Liang, Y., Wu, L., Dong, Y., Reed, S., etal. (2010) Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration. Microb Biotechnol 3: 455-466.
16. +-translocating NADH-quinone reductase from Vibrio alginolyticus. FEBS Lett 488: 5-8.
17. Heidelberg, J.F., Paulsen, I.T., Nelson, K.E., Gaidos, E.J., Nelson, W.C., Read, T.D., etal. (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol 20: 1118-1123.
18. Hunt, K.A., Flynn, J.M., Naranjo, B., Shikhare, I.D., and Gralnick, J.A. (2010) Substrate-level phosphorylation is the primary source of energy conservation during anaerobic respiration of Shewanella oneidensis strain MR-1. J Bacteriol 192: 3345-3351.
19. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
20. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., etal. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
21. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
22. Lawrence, J. (1999) Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr Opin Genet Dev 9: 642-648.
23. Leys, D., Tsapin, A.S., Nealson, K.H., Meyer, T.E., Cusanovich, M.A., and Van Beeumen, J.J. (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1. Nat Struct Biol 6: 1113-1117.
24. Lukk, T., Sakai, A., Kalyanaraman, C., Brown, S.D., Imker, H.J., Song, L., etal. (2012) Homology models guide discovery of diverse enzyme specificities among dipeptide epimerases in the enolase superfamily. Proc Natl Acad Sci USA 109: 4122-4127.
25. MacDonald, M.J., and D'Cunha, G.B. (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85: 273-282.
26. Maier, T.M., Myers, J.M., and Myers, C.R. (2003) Identification of the gene encoding the sole physiological fumarate reductase in Shewanella oneidensis MR-1. J Basic Microbiol 43: 312-327.
27. Mattevi, A., Tedeschi, G., Bacchella, L., Coda, A., Negri, A., and Ronchi, S. (1999) Structure of L-aspartate oxidase: implications for the succinate dehydrogenase/fumarate reductase oxidoreductase family. Structure 7: 745-756.
28. Mehler, A.H., and Tabor, H. (1953) Deamination of histidine to form urocanic acid in liver. J Biol Chem 201: 775-784.
29. Mikoulinskaia, O., Akimenko, V., Galouchko, A., Thauer, R.K., and Hedderich, R. (1999) Cytochrome c-dependent methacrylate reductase from Geobacter sulfurreducens AM-1. Eur J Biochem 263: 346-352.
30. Morris, C.J., Black, A.C., Pealing, S.L., Manson, F.D.C., Chapman, S.K., Reid, G.A., etal. (1994) Purification and properties of a novel cytochrome: flavocytochrome c from Shewanella putrefaciens. Biochem J 302: 587-593.
31. Myers, J.M., and Myers, C.R. (2000) Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J Bacteriol 182: 67-75.
32. Pankhurst, K.L., Mowat, C.G., Rothery, E.L., Hudson, J.M., Jones, A.K., Miles, C.S., etal. (2006) A proton delivery pathway in the soluble fumarate reductase from Shewanella frigidimarina. J Biol Chem 281: 20589-20597.
33. Pennisi, E. (2003) Bioinformatics. Gene counters struggle to get the right answer. Science 301: 1040-1041.
34. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
35. Punta, M., Coggill, P.C., Eberhardt, R.Y., Mistry, J., Tate, J., Boursnell, C., etal. (2012) The Pfam protein families database. Nucleic Acids Res 40(D1): D290-D301.
36. Rahman, O., Cummings, S.P., Harrington, D.J., and Sutcliffe, I.C. (2008) Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol 24: 2377-2382.
37. Ramazzina, I., Cendron, L., Folli, C., Berni, R., Monteverdi, D., Zanotti, G., and Percudani, R. (2008) Logical identification of an allantoinase analog (puuE) recruited from polysaccharide deacetylases. J Biol Chem 283: 23295-23304.
38. Reid, G.A., Miles, C.S., Moysey, R.K., Pankhurst, K.L., and Chapman, S.K. (2000) Catalysis in fumarate reductase. Biochim Biophys Acta 1459: 310-315.
39. Rentzsch, R., and Orengo, C.A. (2009) Protein function prediction - the power of multiplicity. Trends Biotechnol 27: 210-219.
40. Sato, K., Nishina, Y., Setoyama, C., Miura, R., and Shiga, K. (1999) Unusually high standard redox potential of acrylyl-CoA/propionyl-CoA couple among enoyl-CoA/acyl-CoA couples: a reason for the distinct metabolic pathway of propionyl-CoA from longer acyl-CoAs. J Biochem 126: 668-675.
41. Schweikert, G., Behr, J., Zien, A., Zeller, G., Ong, C.S., Sonnenburg, S., etal. (2009) mGene.web: a web service for accurate computational gene finding. Nucleic Acids Res 37: W312-W316.
42. Sen, N.P., McGeer, P.L., and Paul, R.M. (1962) Imidazolepropionic acid as a urinary metabolite of L-histidine. Biochem Biophys Res Commun 9: 257-261.
43. Sucheta, A., Ackrell, B.A., Cochran, B., and Armstrong, F.A. (1992) Diode-like behavior of a mitochondrial electron-transport enzyme. Nature 356: 361-362.
44. Thompson, D.K., Beliaev, A.S., Giometti, C.S., Tollaksen, S.L., Khare, T., Lies, D.P., etal. (2002) Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis: possible involvement of fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl Environ Microbiol 68: 881-892.
45. 3 from Shewanella frigidimarina NCIMB400. Biochemistry 38: 3302-3309.
46. Verkhovsky, M.I., and Bogachev, A.V. (2010) Sodium-translocating NADH:quinone oxidoreductase as a redox-driven ion pump. Biochim Biophys Acta 1797: 738-746.
47. Watanabe, T., and Honda, K. (1982) Measurement of the extinction coefficient of the methyl viologen cation radical and the efficiency of its formation by semiconductor photocatalysis. J Phys Chem 86: 2617-2619.
48. Yeats, C., Bentley, S., and Bateman, A. (2003) New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol 3: ARTN 3.
49. Yu, N.Y., Wagner, J.R., Laird, M.R., Melli, G., Rey, S., Lo, R., etal. (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26: 1608-1615.
50. +-translocating NADH:ubiquinone oxidoreductase from Vibrio harveyi. Biochemistry 38: 16246-16252.