Unexpected abundance of coenzyme F420-dependent enzymes in Mycobacterium tuberculosis and other actinobacteria

Journal of Bacteriology

Volumn 192, Issue 21, 2010, Pages 5788-5798

  Selengut, Jeremy D ^a   Haft, Daniel H ^a  

^a J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; COENZYME F 420 DEPENDENT ENZYME; DEAZAFLAVIN DEPENDENT NITROREDUCTASE; LUCIFERASE LIKE MONOOXYGENASE; PYRIDOXAMINE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; COENZYME; COENZYME F420; FLAVONOID; RIBOFLAVIN;

ARTICLE; BACTERIAL STRAIN; BINDING SITE; BIOSYNTHESIS; CONTROLLED STUDY; INTESTINE FLORA; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATION REDUCTION REACTION; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FUNCTION; ACTINOBACTERIA; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BACTERIAL GENOME; CHEMICAL STRUCTURE; COENZYME; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR BIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN CONFORMATION;

ACTINOBACTERIA; CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA;

ACTINOBACTERIA; AMINO ACID SEQUENCE; BINDING SITES; COENZYMES; FLAVONOIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; MOLECULAR BIOLOGY; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MYCOBACTERIUM TUBERCULOSIS; PHYLOGENY; PROTEIN CONFORMATION; RIBOFLAVIN;

EID: 77958526817     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00425-10     Document Type: Article

References (44)

1. Aufhammer, S. W., E. Warkentin, H. Berk, S. Shima, R. K. Thauer, and U. Ermler. 2004. Coenzyme binding in F420-dependent secondary alcohol dehydrogenase, a member of the bacterial luciferase family. Structure 12:361-370.
2. Aufhammer, S. W., E. Warkentin, U. Ermler, C. H. Hagemeier, R. K. Thauer, and S. Shima. 2005. Crystal structure of methylenetetrahydromethanopterin reductase (Mer) in complex with coenzyme F420: architecture of the F420/FMN binding site of enzymes within the nonprolyl cis-peptide containing bacterial luciferase family. Protein Sci. 14:1840-1849.
3. Bair, T. B., D. W. Isabelle, and L. Daniels. 2001. Structures of coenzyme F(420) in Mycobacterium species. Arch. Microbiol. 176:37-43.
4. Bashiri, G., C. J. Squire, N. J. Moreland, and E. N. Baker. 2008. Crystal structures of F420-dependent glucose-6-phosphate dehydrogenase FGD1 involved in the activation of the anti-tuberculosis drug candidate PA-824 reveal the basis of coenzyme and substrate binding. J. Biol. Chem. 283: 17531-17541.
5. Boshoff, H. I., and C. E. Barry III. 2005. Tuberculosis - metabolism and respiration in the absence of growth. Nat. Rev. Microbiol. 3:70-80.
6. Campbell, Z. T., A. Weichsel, W. R. Montfort, and T. O. Baldwin. 2009. Crystal structure of the bacterial luciferase/flavin complex provides insight into the function of the beta subunit. Biochemistry 48:6085-6094.
7. Canaan, S., G. Sulzenbacher, V. Roig-Zamboni, L. Scappuccini-Calvo, F. Frassinetti, D. Maurin, C. Cambillau, and Y. Bourne. 2005. Crystal structure of the conserved hypothetical protein Rv1155 from Mycobacterium tuberculosis. FEBS Lett. 579:215-221. (Pubitemid 40023399)
8. Chaiyen, P., C. Suadee, and P. Wilairat. 2001. A novel two-protein component flavoprotein hydroxylase. Eur. J. Biochem. 268:5550-5561.
9. Churchich, J. E. 1984. Brain pyridoxine-5-phosphate oxidase. A dimeric enzyme containing one FMN site. Eur. J. Biochem. 138:327-332.
10. Darwin, K. H., S. Ehrt, J. C. Gutierrez-Ramos, N. Weich, and C. F. Nathan. 2003. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:1963-1966.
11. Di Salvo, M., E. Yang, G. Zhao, M. E. Winkler, and V. Schirch. 1998. Expression, purification, and characterization of recombinant Escherichia coli pyridoxine 5′-phosphate oxidase. Protein Expr. Purif. 13:349-356.
12. di Salvo, M. L., M. K. Safo, F. N. Musayev, F. Bossa, and V. Schirch. 2003. Structure and mechanism of Escherichia coli pyridoxine 5′-phosphate oxidase. Biochim. Biophys. Acta 1647:76-82.
13. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
14. Eker, A. P., P. Kooiman, J. K. Hessels, and A. Yasui. 1990. DNA photore-activating enzyme from the cyanobacterium Anacystis nidulans. J. Biol. Chem. 265:8009-8015.
15. Forouhar, F., M. Abashidze, H. Xu, L. L. Grochowski, J. Seetharaman, M. Hussain, A. Kuzin, Y. Chen, W. Zhou, R. Xiao, T. B. Acton, G. T. Montelione, A. Galinier, R. H. White, and L. Tong. 2008. Molecular insights into the biosynthesis of the F420 coenzyme. J. Biol. Chem. 283:11832-11840.
16. Gerlo, E., and E. Schram. 1971. Bioluminescence assay of reduced pyridine and flavine nucleotides with bacterial luciferase. Arch. Int. Physiol. Biochim. 79:200-201.
17. Graham, D. E., H. Xu, and R. H. White. 2003. Identification of the 7,8- didemethyl-8-hydroxy-5-deazariboflavin synthase required for coenzyme F(420) biosynthesis. Arch. Microbiol. 180:455-464.
18. Grochowski, L. L., H. Xu, and R. H. White. 2008. Identification and characterization of the 2-phospho-L-lactate guanylyltransferase involved in coenzyme F420 biosynthesis. Biochemistry 47:3033-3037.
19. Guerra-Lopez, D., L. Daniels, and M. Rawat. 2007. Mycobacterium smegmatis mc2 155 fbiC and MSMEG-2392 are involved in triphenylmethane dye decolorization and coenzyme F420 biosynthesis. Microbiology 153:2724-2732. (Pubitemid 47262061)
20. Haft, D. H., B. J. Loftus, D. L. Richardson, F. Yang, J. A. Eisen, I. T. Paulsen, and O. White. 2001. TIGRFAMs: a protein family resource for the functional identification of proteins. Nucleic Acids Res. 29:41-43.
21. Haft, D. H., I. T. Paulsen, N. Ward, and J. D. Selengut. 2006. Exopolysaccharide- associated protein sorting in environmental organisms: the PEP-CTERM/ EpsH system. Application of a novel phylogenetic profiling heuristic. BMC Biol. 4:29.
22. Kertesz, M. A., K. Schmidt-Larbig, and T. Wuest. 1999. A novel reduced flavin mononucleotide-dependent methanesulfonate sulfonatase encoded by the sulfur-regulated msu operon of Pseudomonas aeruginosa. J. Bacteriol. 181:1464-1473.
23. Kitamura, M., S. Kojima, K. Ogasawara, T. Nakaya, T. Sagara, K. Niki, K. Miura, H. Akutsu, and I. Kumagai. 1994. Novel FMN-binding protein from Desulfovibrio vulgaris (Miyazaki F). Cloning and expression of its gene in Escherichia coli. J. Biol. Chem. 269:5566-5573.
24. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
25. Li, H., M. Graupner, H. Xu, and R. H. White. 2003. CofE catalyzes the addition of two glutamates to F420-0 in F420 coenzyme biosynthesis in Methanococcus jannaschii. Biochemistry 42:9771-9778.
26. Moore, S. A., and M. N. James. 1995. Structural refinement of the nonfluorescent flavoprotein from Photobacterium leiognathi at 1.60 A resolution. J. Mol. Biol. 249:195-214.
27. Onwueme, K. C., C. J. Vos, J. Zurita, C. E. Soll, and L. E. Quadri. 2005. Identification of phthiodiolone ketoreductase, an enzyme required for production of mycobacterial diacyl phthiocerol virulence factors. J. Bacteriol. 187:4760-4766.
28. Parsons, J. F., K. Calabrese, E. Eisenstein, and J. E. Ladner. 2004. Structure of the phenazine biosynthesis enzyme PhzG. Acta Crystallogr. D Biol. Crystallogr. 60:2110-2113.
29. Purwantini, E., and L. Daniels. 1998. Molecular analysis of the gene encoding F420-dependent glucose-6-phosphate dehydrogenase from Mycobacterium smegmatis. J. Bacteriol. 180:2212-2219. (Pubitemid 28212710)
30. Purwantini, E., T. P. Gillis, and L. Daniels. 1997. Presence of F420-dependent glucose-6-phosphate dehydrogenase in Mycobacterium and Nocardia species, but absence from Streptomyces and Corynebacterium species and methanogenic Archaea. FEMS Microbiol. Lett. 146:129-134.
31. Purwantini, E., and B. Mukhopadhyay. 2009. Conversion of NO2 to NO by reduced coenzyme F420 protects mycobacteria from nitrosative damage. Proc. Natl. Acad. Sci. U. S. A. 106:6333-6338.
32. Qin, J., R. Li, J. Raes, M. Arumugam, K. S. Burgdorf, C. Manichanh, T. Nielsen, N. Pons, F. Levenez, T. Yamada, D. R. Mende, J. Li, J. Xu, S. Li, D. Li, J. Cao, B. Wang, H. Liang, H. Zheng, Y. Xie, J. Tap, P. Lepage, M. Bertalan, J. M. Batto, T. Hansen, D. Le Paslier, A. Linneberg, H. B. Nielsen, E. Pelletier, P. Renault, T. Sicheritz-Ponten, K. Turner, H. Zhu, C. Yu, M. Jian, Y. Zhou, Y. Li, X. Zhang, N. Qin, H. Yang, J. Wang, S. Brunak, J. Dore, F. Guarner, K. Kristiansen, O. Pedersen, J. Parkhill, J. Weissenbach, P. Bork, and S. D. Ehrlich. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65.
33. Rusch, D. B., A. L. Halpern, G. Sutton, K. B. Heidelberg, S. Williamson, S. Yooseph, D. Wu, J. A. Eisen, J. M. Hoffman, K. Remington, K. Beeson, B. Tran, H. Smith, H. Baden-Tillson, C. Stewart, J. Thorpe, J. Freeman, C. Andrews-Pfannkoch, J. E. Venter, K. Li, S. Kravitz, J. F. Heidelberg, T. Utterback, Y. H. Rogers, L. I. Falcon, V. Souza, G. Bonilla-Rosso, L. E. Eguiarte, D. M. Karl, S. Sathyendranath, T. Platt, E. Bermingham, V. Gallardo, G. Tamayo-Castillo, M. R. Ferrari, R. L. Strausberg, K. Nealson, R. Friedman, M. Frazier, and J. C. Venter. 2007. The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5:e77.
34. Schroeder, E. K., N. de Souza, D. S. Santos, J. S. Blanchard, and L. A. Basso. 2002. Drugs that inhibit mycolic acid biosynthesis in Mycobacterium tuberculosis. Curr. Pharm. Biotechnol. 3:197-225.
35. Selengut, J. D., D. H. Haft, T. Davidsen, A. Ganapathy, M. Gwinn-Giglio, W. C. Nelson, A. R. Richter, and O. White. 2007. TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res. 35:D260-D264.
36. Selengut, J. D., D. B. Rusch, and D. H. Haft. 2010. Sites inferred by metabolic background assertion labeling (SIMBAL): adapting the partial phylogenetic profiling algorithm to scan sequences for signatures that predict protein function. BMC Bioinformatics 11:52.
37. Shi, R., N. Itagaki, and I. Sugawara. 2007. Overview of anti-tuberculosis (TB) drugs and their resistance mechanisms. Mini Rev. Med. Chem. 7:1177-1185.
38. Simeone, R., P. Constant, W. Malaga, C. Guilhot, M. Daffe, and C. Chalut. 2007. Molecular dissection of the biosynthetic relationship between phthiocerol and phthiodiolone dimycocerosates and their critical role in the virulence and permeability of Mycobacterium tuberculosis. FEBS J. 274:1957-1969. (Pubitemid 46587996)
39. Singh, J. A., R. Upshur, and N. Padayatchi. 2007. XDR-TB in South Africa: no time for denial or complacency. PLoS Med. 4:e50.
40. Singh, R., U. Manjunatha, H. I. Boshoff, Y. H. Ha, P. Niyomrattanakit, R. Ledwidge, C. S. Dowd, I. Y. Lee, P. Kim, L. Zhang, S. Kang, T. H. Keller, J. Jiricek, and C. E. Barry III. 2008. PA-824 kills nonreplicating Mycobacterium tuberculosis by intracellular NO release. Science 322:1392-1395.
41. Thibaut, D., N. Ratet, D. Bisch, D. Faucher, L. Debussche, and F. Blanche. 1995. Purification of the two-enzyme system catalyzing the oxidation of the D-proline residue of pristinamycin IIB during the last step of pristinamycin IIA biosynthesis. J. Bacteriol. 177:5199-5205.
42. Turnbaugh, P. J., M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, R. E. Ley, M. L. Sogin, W. J. Jones, B. A. Roe, J. P. Affourtit, M. Egholm, B. Henrissat, A. C. Heath, R. Knight, and J. I. Gordon. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-484.
43. Winn, M., R. J. Goss, K. Kimura, and T. D. Bugg. 2010. Antimicrobial nucleoside antibiotics targeting cell wall assembly: recent advances in structure-function studies and nucleoside biosynthesis. Nat. Prod. Rep. 27:279-304.
44. Xu, Y., M. W. Mortimer, T. S. Fisher, M. L. Kahn, F. J. Brockman, and L. Xun. 1997. Cloning, sequencing, and analysis of a gene cluster from Chelatobacter heintzii ATCC 29600 encoding nitrilotriacetate monooxygenase and NADH: flavin mononucleotide oxidoreductase. J. Bacteriol. 179:1112-1116. (Pubitemid 27076573)