Comparative genomics guided discovery of two missing archaeal enzyme families involved in the biosynthesis of the pterin moiety of tetrahydromethanopterin and tetrahydrofolate

ACS Chemical Biology

Volumn 7, Issue 11, 2012, Pages 1807-1816

  De Crécy Lagard, Valérie ^a   Phillips, Gabriela ^a   Grochowski, Laura L ^b   Yacoubi, Basma El ^a   Jenney, Francis ^c   Adams, Michael W W ^d   Murzin, Alexey G ^e   White, Robert H ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c PHILADELPHIA COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^d University of Georgia   (United States)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

6 HYDROXYMETHYL 7,8 DIHYDROPTERIN DIPHOSPHATE; 7,8 DIHYDROPTERIN; ARCHAEAL PROTEIN; COG1634 PROTEIN; COG2098 PROTEIN; ENZYME; PTERIDINE DERIVATIVE; PTERIN; PTERIN DERIVATIVE; TETRAHYDROFOLIC ACID; TETRAHYDROMETHANOPTERIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARCHEAN; ARTICLE; BIOTRANSFORMATION; CATALYSIS; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CONVERGENT EVOLUTION; DRUG DESIGN; DRUG SYNTHESIS; ENZYME SPECIFICITY; ENZYME SYNTHESIS; GENETIC ANALYSIS; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ARCHAEA; ARCHAEAL PROTEINS; GENES, ARCHAEAL; GENOMICS; MODELS, MOLECULAR; NEOPTERIN; PHYLOGENY; PTERINS; TETRAHYDROFOLATES;

ARCHAEA;

EID: 84869388277     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300342u     Document Type: Article

References (62)

1. Liolios, K., Chen, I.-M. A., Mavromatis, K., Tavernarakis, N., Hugenholtz, P., Markowitz, V. M., and Kyrpides, N. C. (2010) The Genomes On Line Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata Nucleic Acids Res. 38, D346-D354
2. Overbeek, R., Begley, T., Butler, R. M., Choudhuri, J. V., Chuang, H. Y., Cohoon, M., de Crécy-Lagard, V., Diaz, N., Disz, T., Edwards, R., Fonstein, M., Frank, E. D., Gerdes, S., Glass, E. M., Goesmann, A., Hanson, A., Iwata-Reuyl, D., Jensen, R., Jamshidi, N., Krause, L., Kubal, M., Larsen, N., Linke, B., McHardy, A. C., Meyer, F., Neuweger, H., Olsen, G., Olson, R., Osterman, A., Portnoy, V., Pusch, G. D., Rodionov, D. A., Ruckert, C., Steiner, J., Stevens, R., Thiele, I., Vassieva, O., Ye, Y., Zagnitko, O., and Vonstein, V. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes Nucleic Acids Res. 33, 5691-5702
3. Henry, C. S., Overbeek, R., Xia, F., Best, A. A., Glass, E., Gilbert, J., Larsen, P., Edwards, R., Disz, T., Meyer, F., Vonstein, V., DeJongh, M., Bartels, D., Desai, N., D'Souza, M., Devoid, S., Keegan, K. P., Olson, R., Wilke, A., Wilkening, J., and Stevens, R. L. (2011) Connecting genotype to phenotype in the era of high-throughput sequencing Biochim. Biophys. Acta 1810, 967-977
4. Hanson, A. D., Pribat, A., Waller, J. C., and de Crécy-Lagard, V. (2009) "Unknown" proteins and "orphan" enzymes: the missing half of the engineering parts list and how to find it Biochem. J. 425, 1-11
5. Blaby-Haas, C. E. and de Crécy-Lagard, V. (2011) Mining high-throughput experimental data to link gene and function Trends Biotechnol. 29, 174-182
6. Grochowski, L. L. and White, R. H. (2010) Biosynthesis of the Methanogenic coenzymes. In Comprehensive Natural Products II: Chemistry and Biology (Begley, T., Ed.), pp 711-748, Elsevier, New York.
7. Maden, B. E. (2000) Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism Biochem. J. 350, 609-629
8. Chistoserdova, L., Vorholt, J. A., Thauer, R. K., and Lidstrom, M. E. (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea Science 281, 99-102
9. Ortenberg, R., Rozenblatt-Rosen, O., and Mevarech, M. (2000) The extremely halophilic archaeon Haloferax volcanii has two very different dihydrofolate reductases Mol. Microbiol. 35, 1493-1505
10. White, R. H. (1991) Distribution of folates and modified folates in extremely thermophilic bacteria J. Bacteriol. 173, 1987-1991
11. White, R. H. (1993) Structures of the modified folates in the extremely thermophilic archaebacterium Thermococcus litoralis J. Bacteriol. 175, 3661-3663
12. White, R. H. (1993) Structures of the modified folates in the thermophilic archaebacteria Pyrococcus furiosus Biochemistry 32, 745-753
13. White, R. H. (1997) Purine biosynthesis in the domain Archaea without folates or modified folates J. Bacteriol. 179, 3374-3377
14. Thauer, R. (1997) Biodiversity and unity in biochemistry Antonie van Leeuwenhoek 71, 21-32
15. Buchenau, B. and Thauer, R. K. (2004) Tetrahydrofolate-specific enzymes in Methanosarcina barker i; and growth dependence of this methanogenic archaeon on folic acid or p -aminobenzoic acid Arch. Microbiol. 182, 313-325
16. Zhou, D. and White, R. H. (1992) 5-(p -Aminophenyl)-1,2,3,4- tetrahydroxypentane, a structural component of the modified folate in Sulfolobus solfataricus J. Bacteriol. 174, 4576-4582
17. Graham, D. E. and White, R. H. (2002) Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics Nat. Prod. Rep. 19, 133-147
18. Yim, J. J. and Brown, G. M. (1976) Characteristics of guanosine triphosphate cyclohydrolase I purified from Escherichia coli J. Biol. Chem. 251, 5087-5094
19. Nar, H., Huber, R., Auerbach, G., Fischer, M., Hosl, C., Ritz, H., Bracher, A., Meining, W., Eberhardt, S., and Bacher, A. (1995) Active site topology and reaction mechanism of GTP cyclohydrolase I Proc. Natl. Acad. Sci. U.S.A. 92, 12120-12125
20. El Yacoubi, B., Bonnett, S., Anderson, J. N., Swairjo, M. A., Iwata-Reuyl, D., and de Crécy-Lagard, V. (2006) Discovery of a new prokaryotic type I GTP cyclohydrolase family J. Biol. Chem. 281, 37586-37593
21. Garcon, A., Levy, C., and Derrick, J. P. (2006) Crystal structure of the bifunctional dihydroneopterin aldolase/6-hydroxymethyl-7,8-dihydropterin pyrophosphokinase from Streptococcus pneumoniae J. Mol. Biol. 360, 644-653
22. Dittrich, S., Mitchell, S. L., Blagborough, A. M., Wang, Q., Wang, P., Sims, P. F. G., and Hyde, J. E. (2008) An atypical orthologue of 6-pyruvoyltetrahydropterin synthase can provide the missing link in the folate biosynthesis pathway of malaria parasites Mol. Microbiol. 67, 609-618
23. Hyde, J. E., Dittrich, S., Wang, P., Sims, P. F., de Crécy-Lagard, V., and Hanson, A. D. (2008) Plasmodium falciparum: a paradigm for alternative folate biosynthesis in diverse microorganisms? Trends Parisitol. 24, 502-508
24. Pribat, A., Jeanguenin, L., Lara-Nunez, A., Ziemak, M. J., Hyde, J. E., de Crécy-Lagard, V., and Hanson, A. D. (2009) 6-Pyruvoyltetrahydropterin synthase paralogs replace the folate synthesis enzyme dihydroneopterin aldolase in diverse bacteria J. Bacteriol. 191, 4158-4165
25. Talarico, T. L., Ray, P. H., Dev, I. K., Merrill, B. M., and Dallas, W. S. (1992) Cloning, sequence analysis, and overexpression of Escherichia coli folK, the gene coding for 7,8-dihydro-6-hydroxymethylpterin-pyrophosphokinase J. Bacteriol. 174, 5971-5977
26. Bult, C. J., White, O., Olsen, G. J., Zhou, L., Fleischmann, R. D., Sutton, G. G., Blake, J. A., FitzGerald, L. M., Clayton, R. A., Gocayne, J. D., Kerlavage, A. R., Dougherty, B. A., Tomb, J. F., Adams, M. D., Reich, C. I., Overbeek, R., Kirkness, E. F., Weinstock, K. G., Merrick, J. M., Glodek, A., Scott, J. L., Geoghagen, N. S. M., Weidman, J. F., Fuhrmann, J. L., and Venter, J. C. (1996) Complete genome sequence of the methanogenic archaeon Methanococcus jannaschii Science 273, 1058-1073
27. Phillips, G., El Yacoubi, B., Lyons, B., Alvarez, S., Iwata-Reuyl, D., and de Crécy-Lagard, V. (2008) Biosynthesis of 7-deazaguanosine-modified tRNA nucleosides: a new role for GTP Cyclohydrolase I J. Bacteriol. 190, 7876-7884
28. El Yacoubi, B., Phillips, G., Blaby, I. K., Haas, C. E., Cruz, Y., Greenberg, J., and de Crécy-Lagard, V. (2009) A gateway platform for functional genomics in Haloferax volcanii: deletion of three tRNA modification genes Archaea 2, 211-219
29. 2+-dependent Archaeal-specific GTP Cyclohydrolase, MptA, from Methanocaldococcus jannaschii Biochemistry 46, 6658-6667
30. 2+- dependent cyclic phosphodiesterase catalyzes the hydrolysis of 7,8-dihydro- d -neopterin 2′,3′-cyclic phosphate in methanopterin biosynthesis Biochemistry 48, 9384-9392
31. Phillips, G., Grochowski, L. L., Bonnett, S., Xu, H., Bailly, M., Blaby-Haas, C., El Yacoubi, B., Iwata-Reuyl, D., White, R. H., and de Crécy-Lagard, V. (2012) Functional promiscuity of the COG0720 family ACS Chem. Biol. 7, 197-209
32. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., and Bryant, S. H. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins Nucleic Acids Res. 39, D225-D229
33. Nosaka, K., Kaneko, Y., Nishimura, H., and Iwashima, A. (1993) Isolation and characterization of a thiamin pyrophosphokinase gene, THI80, from Saccharomyces cerevisiae J. Biol. Chem. 268, 17440-17447
34. Baker, L. J., Dorocke, J. A., Harris, R. A., and Timm, D. E. (2001) The crystal structure of yeast thiamin pyrophosphokinase Structure 9, 539-546
35. Timm, D. E., Liu, J., Baker, L. J., and Harris, R. A. (2001) Crystal structure of thiamin pyrophosphokinase J. Mol. Biol. 310, 195-204
36. Santini, S., Monchois, V., Mouz, N., Sigoillot, C., Rousselle, T., Claverie, J.-M., and Abergel, C. (2008) Structural characterization of CA1462, the Candida albicans thiamine pyrophosphokinase BMC Struct. Biol. 8, 33
37. Liu, J. Y. and Hurley, T. D. (2011) A new crystal form of mouse thiamin pyrophosphokinase Int. J. Biochem. Mol. Biol. 2, 111-118
38. Jaroszewski, L., Li, Z., Cai, X.-H., Weber, C., and Godzik, A. (2011) FFAS server: novel features and applications Nucleic Acids Res. 39, W38-W44
39. Chiu, C. P., Watts, A. G., Lairson, L. L., Gilbert, M., Lim, D., Wakarchuk, W. W., Withers, S. G., and Strynadka, N. C. (2004) Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog Nat. Struct. Mol. Biol. 11, 163-170
40. Rao, F. V., Rich, J. R., Rakic, B., Buddai, S., Schwartz, M. F., Johnson, K., Bowe, C., Wakarchuk, W. W., Defrees, S., Withers, S. G., and Strynadka, N. C. (2009) Structural insight into mammalian sialyltransferases Nat. Struct. Mol. Biol. 16, 1186-1188
41. Mashhadi, Z., Zhang, H., Xu, H., and White, R. H. (2008) Identification and characterization of an Archaeon-specific riboflavin kinase J. Bacteriol. 190, 2615-2618
42. Mashhadi, Z., Xu, H., Grochowski, L. L., and White, R. H. (2010) Archaeal RibL: a new FAD synthetase that is air sensitive Biochemistry 49, 8748-8755
43. Wang, Y., Li, Y., and Yan, H. (2006) Mechanism of dihydroneopterin aldolase: functional roles of the conserved active site glutamate and lysine residues Biochemistry 45, 15232-15239
44. BAD promoter J. Bacteriol. 177, 4121-4130
45. Jönsson, M. and Swedberg, G. (2005) Hydroxymethyldihydropterin pyrophosphokinase from Plasmodium falciparum complements a folK -knockout mutant in E. coli when expressed as a separate polypeptide detached from dihydropteroate synthase Mol. Biochem. Parasitol. 140, 123-125
46. Klaus, S. M., Kunji, E. R., Bozzo, G. G., Noiriel, A., de la Garza, R. D., Basset, G. J., Ravanel, S., Rebeille, F., Gregory, J. F., III, and Hanson, A. D. (2005) Higher plant plastids and cyanobacteria have folate carriers related to those of trypanosomatids J. Biol. Chem. 280, 38457-38463
47. Waters, E., Hohn, M. J., Ahel, I., Graham, D. E., Adams, M. D., Barnstead, M., Beeson, K. Y., Bibbs, L., Bolanos, R., Keller, M., Kretz, K., Lin, X., Mathur, E., Ni, J., Podar, M., Richardson, T., Sutton, G. G., Simon, M., SÃll, D., Stetter, K. O., Short, J. M., and Noordewier, M. (2003) The genome of Nanoarchaeum equitan s: Insights into early archaeal evolution and derived parasitism Proc. Natl. Acad. Sci. U.S.A. 100, 12984-12988
48. Gorris, L. G., Voet, A. C., and van der Drift, C. (1991) Structural characteristics of methanogenic cofactors in the non-methanogenic archaebacterium Archaeoglobus fulgidus Biofactors 3, 29-35
49. White, R. H. (1988) Analysis and characterization of the folates in the nonmethanogenic archaebacteria J. Bacteriol. 170, 4608-4612
50. Galperin, M. Y. and Koonin, E. V. (2012) Divergence and convergence in enzyme evolution J. Biol. Chem. 287, 21-28
51. Samuel, B. S., Hansen, E. E., Manchester, J. K., Coutinho, P. M., Henrissat, B., Fulton, R., Latreille, P., Kim, K., Wilson, R. K., and Gordon, J. I. (2007) Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut Proc. Natl. Acad. Sci. U.S.A. 104, 10643-10648
52. Horz, H.-P. and Conrads, G. (2010) The discussion goes on: what is the role of Euryarchaeota in humans? Archaea 2010, 967271
53. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool J. Mol. Biol. 215, 403-410
54. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., and Thompson, J. D. (2003) Multiple sequence alignment with the Clustal series of programs Nucleic Acids Res. 31, 3497-3500
55. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15, 305-308
56. Kitagawa, M., Ara, T., Arifuzzaman, M., Ioka-Nakamichi, T., Inamoto, E., Toyonaga, H., and Mori, H. (2005) Complete set of ORF clones of Escherichia coli ASKA library (A complete set of E. coli K-12 ORF archive): unique resources for biological research DNA Res. 12, 291-299
57. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
58. Sugar, F., Jenney, F., Poole, F., Brereton, P., Izumi, M., Shah, C., and Adams, M. (2005) Comparison of small- and large-scale expression of selected Pyrococcus furiosus genes as an aid to high-throughput protein production J. Struct. Funct. Genomics 6, 149-158
59. Xu, H., Aurora, R., Rose, G. D., and White, R. H. (1999) Identifying two ancient enzymes in Archaea using predicted secondary structure alignment Nat. Struct. Mol. Biol. 6, 750-754
60. Scott, J. W. and Rasche, M. E. (2002) Purification, overproduction, and partial characterization of β-RFAP synthase, a key enzyme in the methanopterin biosynthesis pathway J. Bacteriol. 184, 4442-4448
61. Levin, I., Giladi, M., Altman-Price, N., Ortenberg, R., and Mevarech, M. (2004) An alternative pathway for reduced folate biosynthesis in bacteria and halophilic archaea Mol. Microbiol. 54, 1307-1318
62. Li, H., Graupner, M., Xu, H., and White, R. H. (2003) CofE catalyzes the addition of two glutamates to F420-0 in F420 coenzyme biosynthesis in Methanococcus jannaschii Biochemistry 42, 9771-9778