Cyanuric acid hydrolase: Evolutionary innovation by structural concatenation

Molecular Microbiology

Volumn 88, Issue 6, 2013, Pages 1149-1163

  Peat, Thomas S ^a   Balotra, Sahil ^a   Wilding, Matthew ^a   French, Nigel G ^a   Briggs, Lyndall J ^a   Panjikar, Santosh ^b,c   Cowieson, Nathan ^b   Newman, Janet ^a   Scott, Colin ^a  

^a CSIRO   (Australia)

^b AUSTRALIAN SYNCHROTRON   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; BARBITURASE; BARBITURIC ACID; CYANURIC ACID; CYANURIC ACID HYDROLASE; MELAMINE; MONOMER; MUTANT PROTEIN; PEPTIDES AND PROTEINS; PHOSPHATE; UNCLASSIFIED DRUG; WILD TYPE PROTEIN;

ARTICLE; BETA SHEET; BINDING SITE; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SPECIFICITY; HYDROGEN BOND; METAL BINDING; MOLECULAR EVOLUTION; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MODIFICATION; SEQUENCE HOMOLOGY; STRUCTURAL CONCATENATION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TOBLERONE FOLD; X RAY CRYSTALLOGRAPHY;

AMIDOHYDROLASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; ENZYME INHIBITORS; MODELS, MOLECULAR; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; TRIAZINES;

EID: 84879008037     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12249     Document Type: Article

References (44)

1. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
2. Botos, I., and Wlodawer, A. (2007) The expanding diversity of serine hydrolases. Curr Opin Struct Biol 17: 683-690.
3. Burman, J.D., Stevenson, C.E.M., Sawers, R.G., and Lawson, D.M. (2007) The crystal structure of Escherichia coli TdcF, a member of the highly conserved YjgF/YER057c/UK114 family. BMC Struct Biol 7: 30.
4. Cowtan, K. (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011.
5. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
6. Dudev, T., Cowan, J.A., and Lim, C. (1999) Competitive binding in magnesium coordination chemistry: water versus ligands of biological interest. J Am Chem Soc 121: 7665-7673.
7. Ekici, O.D., Paetzel, M., and Dalbey, R.E. (2008) Unconventional serine proteases: variations on the catalytic Ser/His/Asp triad configuration. Protein Sci 17: 2023-2037.
8. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010) Features and development of coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
9. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
10. Fruchey, I., Shapir, N., Sadowsky, M.J., and Wackett, L. (2003) On the origins of cyanuric acid hydrolase: purification, substrates, and prevalence of AtzD from Pseudomonas sp strain ADP. Appl Environ Microbiol 69: 3653-3657.
11. Golovacheva, R.S., and Karavaiko, G.I. (1978) New genus of thermophilic spore-forming bacteria, Sulfobacillus. Microbiology 47: 658-665.
12. Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C., and Vonk, A. (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Perspect 111: 568-575.
13. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain-reaction. Gene 77: 51-59.
14. Kabsch, W. (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
15. Karavajko, G.I., Bulygina, E.S., Tsaplina, I.A., Bogdanova, T.I., and Chumakov, K.M. (1990) Sulfobacillus thermonsulfoidooxidans - a new lineage of bacterial evolution. FEBS Lett 261: 8-10.
16. Karns, J.S. (1999) Gene sequence and properties of an s-triazine ring-cleavage enzyme from Pseudomonas sp. strain NRRLB-12227. Appl Environ Microbiol 65: 3512-3517.
17. Kim, J.M., Yoshikawa, H., and Shirahige, K. (2001) A member of the YER057c/yjgf/Uk114 family links isoleucine biosynthesis and intact mitochondria maintenance in Saccharomyces cerevisiae. Genes Cells 6: 507-517.
18. Knapik, A.A., Petkowski, J.J., Otwinowski, Z., Cymborowski, M.T., Cooper, D.R., Chruszcz, M., etal. (2012) Structure of Escherichia coli RutC, a member of the YjgF family and putative aminoacrylate peracid reductase of the rut operon. Acta Crystallograph Sect F Struct Biol Cryst Commun 68: 1294-1299.
19. Kovalenko, E.V., and Malakhova, P.T. (1983) The spore-forming iron-oxidizing bacterium Sulfobacillus thermosulfidooxidans. Microbiology 52: 760-763.
20. Lennox, E.S. (1955) Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1: 190-206.
21. Letunic, I., and Bork, P. (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128.
22. Letunic, I., and Bork, P. (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475-W478.
23. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
24. McKinney, M.K., and Cravatt, B.F. (2003) Evidence for distinct roles in catalysis for residues of the serine-serine-lysine catalytic triad of fatty acid amide hydrolase. J Biol Chem 278: 37393-37399.
25. MacLennan, P.A., Delzell, E., Sathiakumar, N., Myers, S.L., Cheng, H., Grizzle, W., etal. (2002) Cancer incidence among triazine herbicide manufacturing workers. J Occup Environ Med 44: 1048-1058.
26. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
27. Narayan, S.J., and Sahana, S. (2009) Bioleaching: a review. Res J Biotechnol 4: 72-75.
28. Noor, S., Taylor, M.C., Russell, R.J., Jermiin, L.S., Jackson, C.J., Oakeshott, J.G., and Scott, C. (2012) Intramolecular epistasis and the evolution of a new enzymatic function. PLoS ONE 7: e39822. doi:10.1371/journal.pone.0039822
29. Paetzel, M., Dalbey, R.E., and Strynadka, N.C.J. (1998) Crystal structure of a bacterial signal peptidase in complex with a beta-lactam inhibitor. Nature 396: 186-190.
30. Panjikar, S., Parthasarathy, V., Lamzin, V.S., Weiss, M.S., and Tucker, P.A. (2005) Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr D Biol Crystallogr 61: 449-457.
31. Pratt, R.F., and McLeish, M.J. (2010) Structural relationship between the active sites of beta-lactam-recognizing and amidase signature enzymes: convergent evolution? Biochemistry 49: 9688-9697.
32. Schaap, F.G., van der Vusse, G.J., and Glatz, J.F.C. (2002) Evolution of the family of intracellular lipid binding proteins in vertebrates. Mol Cell Biochem 239: 69-77.
33. Seffernick, L.J., Sadowsky, M.J., and Wackett, L.P. (2009) Thermostable cyanuric acid hydrolase from Moorella thermoacetica ATCC 39073. Appl Environ Microbiol 75: 6986-6991.
34. Seffernick, L.J., Erickson, J.S., Cameron, S.M., Cho, S., Dodge, A.G., Richman, J.E., etal. (2012) Defining sequence space and reaction products within the cyanuric acid hydrolase (AtzD)/barbiturase protein family. J Bacteriol 194: 4579-4588.
35. Soong, C.L., Ogawa, J., and Shimizu, S. (2001) Novel amidohydrolytic reactions in oxidative pyrimidine metabolism: analysis of the barbiturase reaction and discovery of a novel enzyme, ureidomalonase. Biochem Biophys Res Commun 286: 222-226.
36. Soong, C.L., Ogawa, J., Sakuradani, E., and Shimizu, S. (2002) Barbiturase, a novel zinc-containing amidohydrolase involved in oxidative pyrimidine metabolism. J Biol Chem 277: 7051-7058.
37. Svergun, D., Barberato, C., and Koch, M.H.J. (1995) CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 28: 768-773.
38. Tang, K., Baskaran, V., and Nemati, M. (2009) Bacteria of the sulphur cycle: an overview of microbiology, biokinetics and their role in petroleum and mining industries. Biochem Eng J 44: 73-94.
39. Temple, K.L., and Colmer, A.R. (1951) The autotrophic oxidation of iron by a new bacterium Thiobacillus ferrooxidans. J Bacteriol 62: 605-611.
40. Udikovic-Kolic, N., Scott, C., and Martin-Laurent, F. (2012) Evolution of atrazine-degrading capabilities in the environment. Appl Microbiol Biotechnol 96: 1175-1189.
41. Wackett, L.P. (2009) Questioning our perceptions about evolution of biodegradative enzymes. Curr Opin Microbiol 12: 244-251.
42. Waksman, S.A., and Joffe, J.S. (1922) Microorganisms concerned in the oxidation of sulfur in the soil II. Thiobacillus thiooxidans, a new sulfur-oxidizing organism isolated from the soil. J Bacteriol 7: 239-256.
43. Wiegand, C., Krause, E., Steinberg, C., and Pflugmacher, S. (2001) Toxicokinetics of atrazine in embryos of the zebrafish (Danio rerio). Ecotoxicol Environ Saf 49: 199-205.
44. Zhang, H.M., Gao, Y., Li, M., and Chang, W.R. (2010) Crystal structure of the PSPTO-PSP protein from Pseudomonas syringae pv. tomato str. DC3000 in complex with d-glucose. Biochem Biophys Res Commun 397: 82-86.