Abstract
Enzymes are central to the biology of many pesticides, influencing their modes of action, environmental fates and mechanisms of target species resistance. Since the introduction of synthetic xenobiotic pesticides, enzymes responsible for pesticide turnover have evolved rapidly, in both the target organisms and incidentally exposed biota. Such enzymes are a source of significant biotechnological potential and form the basis of several bioremediation strategies intended to reduce the environmental impacts of pesticide residues. This review describes examples of enzymes possessing the major activities employed in the bioremediation of pesticide residues, and some of the strategies by which they are employed. In addition, several examples of specific achievements in enzyme engineering are considered, highlighting the growing trend in tailoring enzymatic activity to a specific biotechnologically relevant function.
Keywords: Bacterial enzymes, Bioremediation, Pesticides, Xenobiotics
Full Text
The Full Text of this article is available as a PDF (203.2 KB).
References
- 1.Shapir N., Mongodin E.F., Sadowsky M.J., Daugherty S.C., Nelson K.E., Wackett L.P. Evolution of catabolic pathways: Genomic insights into microbial s-triazine metabolism. J Bacteriol. 2007;189:674–682. doi: 10.1128/JB.01257-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Jorgensen K.S. In situ bioremediation. Adv Appl Microbiol. 2007;61:285–305. doi: 10.1016/S0065-2164(06)61008-3. [DOI] [PubMed] [Google Scholar]
- 3.Alcalde M., Ferrer M., Plou F.J., Ballesteros A. Environmental biocatalysis: from remediation with enzymes to novel green processes. Trends Biotechnol. 2006;24:281–287. doi: 10.1016/j.tibtech.2006.04.002. [DOI] [PubMed] [Google Scholar]
- 4.Sutherland T.D., Horne I., Weir K.M., Coppin C.W., Williams M.R., Selleck M., Russell R.J., Oakeshott J.G. Enzymatic bioremediation: From enzyme discovery to applications. Clinic Exper Pharmacol Physiol. 2004;31:817–821. doi: 10.1111/j.1440-1681.2004.04088.x. [DOI] [PubMed] [Google Scholar]
- 5.Barry GF and Kishore GM (1992) Glyphosate tolerant plants. Patent WO92/00377
- 6.Barry GF and Kishore GM (1998) Glyphosate tolerant plants. Patent US 5,776,760
- 7.Settembre E.C., Dorrestein P.C., Park J.H., Augustine A.M., Begley T.P., Ealick S.E. Structural and mechanistic studies on ThiO, a glycine oxidase essential for thiamin biosynthesis in Bacillus subtilis. Biochem. 2003;42:2971–2981. doi: 10.1021/bi026916v. [DOI] [PubMed] [Google Scholar]
- 8.Joosten V., Berkel W.J.H. Flavoenzymes. Curr Opin Chem Biol. 2007;11:195–202. doi: 10.1016/j.cbpa.2007.01.010. [DOI] [PubMed] [Google Scholar]
- 9.Galan B., Diaz E., Prieto M.A., Garcia J.L. Functional analysis of the small component of the 4-hydroxyphenylacetate 3-monooxygenase of Escherichia coli W: a prototype of a new flavin: NAD(P)H reductase subfamily. J Bacteriol. 2000;182:627–636. doi: 10.1128/JB.182.3.627-636.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Goebel G., Gorbach S., Knauf W., Rimpau R.H., Huttenbach H. Properties, effects, residues, and analytics of the insecticide endosulfan. Residue Rev. 1982;83:1–165. doi: 10.1007/978-1-4612-5712-7_1. [DOI] [PubMed] [Google Scholar]
- 11.Sutherland T.D., Horne I., Weir K.M., Russell R.J., Oakeshott J.G. Toxicity and residues of endosulfan isomers. Reviews Environ Contamin Toxicol. 2004;183:99–113. doi: 10.1007/978-1-4419-9100-3_4. [DOI] [PubMed] [Google Scholar]
- 12.Sutherland T.D., Horne I., Lacey M.J., Harcourt R.L., Russell R.J., Oakeshott J.G. Enrichment of an endosulfandegrading mixed bacterial culture. Appl Environ Microbiol. 2000;66:2822–2828. doi: 10.1128/AEM.66.7.2822-2828.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Sutherland T.D., Weir K.M., Lacey M.J., Horne I., Russell R.J., Oakeshott J.G. Enrichment of a microbial culture capable of degrading endosulphate, the toxic metabolite of endosulfan. J Appl Microbiol. 2002;92:541–548. doi: 10.1046/j.1365-2672.2002.01559.x. [DOI] [PubMed] [Google Scholar]
- 14.Weir K.M., Sutherland T.D., Horne I., Russell R.J., Oakeshott J.G. A single monooxygenase, ese, is involved in the metabolism of the organochlorides endosulfan and endosulfate in an Arthrobacter sp. Appl Environ Microbiol. 2006;72:3524–3530. doi: 10.1128/AEM.72.5.3524-3530.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Sutherland T.D., Horne I., Harcourt R.L., Russell R.J., Oakeshott J.G. Isolation and characterization of a Mycobacterium strain that metabolizes the insecticide endosulfan. J Appl Microbiol. 2002;93:380–389. doi: 10.1046/j.1365-2672.2002.01728.x. [DOI] [PubMed] [Google Scholar]
- 16.Sutherland T.D., Horne I., Russell R.J., Oakeshott J.G. Gene cloning and molecular characterization of a two-enzyme system catalyzing the oxidative detoxification of beta-endosulfan. Appl Environ Microbiol. 2002;68:6237–6245. doi: 10.1128/AEM.68.12.6237-6245.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Werck-Reichhart D., Hehn A., Didierjean L. Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci. 2000;5:116–123. doi: 10.1016/S1360-1385(00)01567-3. [DOI] [PubMed] [Google Scholar]
- 18.Urlacher V.B., Lutz-Wahl S., Schmid R.D. Microbial P450 enzymes in biotechnology. Appl Microbiol Biotechnol. 2004;64:317–325. doi: 10.1007/s00253-003-1514-1. [DOI] [PubMed] [Google Scholar]
- 19.Morant M., Bak S., Moller B.L., Werck-Reichhart D. Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol. 2003;14:151–162. doi: 10.1016/S0958-1669(03)00024-7. [DOI] [PubMed] [Google Scholar]
- 20.Klingenberg M. The dragging emergence of the P450 cytochrome. Arch Biochem Biophys. 2003;412:2. doi: 10.1016/S0003-9861(03)00060-2. [DOI] [PubMed] [Google Scholar]
- 21.Kawahigashi H., Hirose S., Ohkawa H., Ohkawa Y. Transgenic rice plants expressing human CYP1A1 remediate the triazine herbicides atrazine and simazine. J Agric Food Chem. 2005;53:8557–8564. doi: 10.1021/jf051370f. [DOI] [PubMed] [Google Scholar]
- 22.Kawahigashi H., Hirose S., Ohkawa H., Ohkawa Y. Herbicide resistance of transgenic rice plans expressing human CYP1A1. Biotechnol Adv. 2007;25:75–84. doi: 10.1016/j.biotechadv.2006.10.002. [DOI] [PubMed] [Google Scholar]
- 23.Yamada T., Ishige T., Shiota N., Inui H., Ohkawa H., Ohkawa Y. Enhancement of metabolizing herbicides in young tubers of transgenic potato plants with the rat CYP1A1 gene. Theoret Appl Genet. 2002;105:515–520. doi: 10.1007/s00122-002-0961-x. [DOI] [PubMed] [Google Scholar]
- 24.Hanioka N., Tatarazako N., Jinno H., Arizono K., Ando M. Determination of cytochrome P450 1A activities in mammalian liver microsomes by high-performance liquid chromatography with fluorescence detection. J Chromatograph B. 2000;744:399–406. doi: 10.1016/S0378-4347(00)00278-4. [DOI] [PubMed] [Google Scholar]
- 25.Kawahigashi H., Hirose S., Ohkawa H., Ohkawa Y. Phytoremediation of the herbicides atrazine and metolachlor by transgenic rice plants expressing human CYP1A1, CYP2B6, and CYP2C19. J Agric Food Chem. 2006;54:2985–2991. doi: 10.1021/jf052610u. [DOI] [PubMed] [Google Scholar]
- 26.Didierjean L., Gondet L., Perkins R., Lau S.M.C., Schaller H., O’Keefe D.P., Werck-Reichhart D. Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiol. 2002;130:179–189. doi: 10.1104/pp.005801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Chen X., Christopher A., Jones J.P., Bell S.G., Guo Q., Xu F., Roa Z., Wong L.L. Crystal structure of the F87W/Y96F/V247L mutant of cytochrome P-450cam with 1,3,5-trichlorobenzene bound and further protein engineering for the oxidation of pentachlorobenzene and hexachlorobenezene. J Biol Chem. 2002;277:37519–37526. doi: 10.1074/jbc.M203762200. [DOI] [PubMed] [Google Scholar]
- 28.Yan D.Z., Lui H., Zhou N.Y. Conversion of Sphingobium chlorophenolicum ATCC 39723 to a hexachlorobenzene degrader by metabolic engineering. Appl Environ Microbiol. 2006;72:2283–2286. doi: 10.1128/AEM.72.3.2283-2286.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Yeh W.K., Gibson D.T., Liu T.N. Toluene dioxygenase: a multicomponent enzyme system. Biochem Biophys Res Comm. 1977;78:401–410. doi: 10.1016/0006-291X(77)91268-2. [DOI] [PubMed] [Google Scholar]
- 30.Gibson D.T., Yeh W.K., Liu T.N., Subramanian V. In: Oxygenases and Oxygen Metabolism. Nozaki M., Yamamoto S., Ishimura Y., Coon M.J., Ernster L., Estabrook R.W., editors. New York: Academic Press, Inc.; 1982. pp. 51–62. [Google Scholar]
- 31.Whited G.M., Gibson D.T. Toluene-4-monooxygenase, a 3-component enzyme-system that catalyzes the oxidation of toluene to para-cresol in Pseudomonas mendocina KR1. J Bacteriol. 1991;173:3010–3016. doi: 10.1128/jb.173.9.3010-3016.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Bui V.P., Hansen T.V., Stenstrom Y., Hudlicky T., Ribbons D.W. A study of substrate specificity of toluene dioxygenase in processing aromatic compounds containing benzylic and/or remote chiral centers. J Chem. 2001;25:116–124. [Google Scholar]
- 33.Robertson J.B., Spain J.C., Haddock J.D., Gibson D.T. Oxidation of nitrotoluenes by toluene dioxygenase — evidence for a monooxygenase reaction. Appl Environ Microbiol. 1992;58:2643–2648. doi: 10.1128/aem.58.8.2643-2648.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Lang C.C., Wackett L.P. Oxidation of aliphatic olefins by toluene dioxygenase: enzyme rates and product identification. J Bacteriol. 1997;179:3858–3865. doi: 10.1128/jb.179.12.3858-3865.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Resnick S.M., Lee K., Gibson D.T. Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp strain NCIB 9816. J Indust Microbiol Biotechnol. 1996;17:438–457. doi: 10.1007/BF01574775. [DOI] [Google Scholar]
- 36.Subramanian V., Liu T.N., Yeh W.K., Narro M., Gibson D.T. Purification and properties of NADH-ferredoxintol reductase — a component of toluene dioxygenase from Pseudomonas putida. J Biol Chem. 1981;256:2723–2730. [PubMed] [Google Scholar]
- 37.Subramanian V., Liu T.N., Yeh W.K., Serdar C.M., Wackett L.P., Gibson D.T. Purification and properties of ferredoxintol — a component of toluene dioxygenase from Pseudomonas putida F1. J Biol Chem. 1985;260:2355–2363. [PubMed] [Google Scholar]
- 38.Subramanian V., Liu T.N., Yeh W.K., Gibson D.T. Toluene dioxygenase — purification of an iron-sulfur protein by affinity-chromatography. Biochem Biophys Res Comm. 1979;91:1131–1139. doi: 10.1016/0006-291x(79)91998-3. [DOI] [PubMed] [Google Scholar]
- 39.Zylstra G.J., Gibson D.T. Toluene degradation by Pseudomonas putida F1 — nucleotide-sequence of the todc1c2BADE genes and their expression in Escherichiacoli. J Biol Chem. 1989;264:14940–14946. [PubMed] [Google Scholar]
- 40.Parales R.E., Huang R., Yu C.L., Parales J.V., Lee F.K.N., Lessner D.J., Ivkovic-Jensen M.M., Liu W., Friemann R., Ramaswamy S., Gibson D.T. Purification, characterization, and crystallization of the components of the nitrobenzene and 2-nitrotoluene dioxygenase enzyme systems. Appl Environ Microbiol. 2005;71:3806–3814. doi: 10.1128/AEM.71.7.3806-3814.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Newman L.M., Wackett L.P. Purification and characterization of toluene 2-monooxygenase from Burkholderia cepacia G4. Biochem. 1995;34:14066–14076. doi: 10.1021/bi00043a012. [DOI] [PubMed] [Google Scholar]
- 42.Newman L.M., Wackett L.P. Trichloroethylene oxidation by purified toluene 2-monooxygenase: products, kinetics, and turnover-dependent inactivation. J Bacteriol. 1997;197:90–96. doi: 10.1128/jb.179.1.90-96.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Ferraro D.J., Gakhar L., Ramaswamy S. Rieske business: Structure-function of Rieske non-heme oxygenases. Biochem Biophys Res Comm. 2005;338:175–190. doi: 10.1016/j.bbrc.2005.08.222. [DOI] [PubMed] [Google Scholar]
- 44.Taira K., Hirose J., Hayashid S., Furukawa K. Analysis of bph operon from the polychlorinated biphenyldegrading strain of Pseudomonas pseudoalcaligenes KF707. J Biol Chem. 1992;267:8488–4853. [PubMed] [Google Scholar]
- 45.Maeda T., Takahashi Y., Suenaga H., Suyama A., Goto M., Furukawa K. Functional analyses of Bph-Tod hybrid dioxygenase, which exhibits high degradation activity toward trichloroethylene. J Biol Chem. 2001;276:29833–29838. doi: 10.1074/jbc.M102025200. [DOI] [PubMed] [Google Scholar]
- 46.Furukawa K., Hirose J., Hayashida S., Nakamura K. Efficient degradation of trichloroethylene by a hybrid aromatic ring dioxygenase. J Bacteriol. 1994;196:2121–2123. doi: 10.1128/jb.176.7.2121-2123.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Ollis D.L., Cheah E., Cygler M., Dijkstra B., Frolow F., Franken S.M., Harel M., Remington S.J., Silman I., Schrag J., Sussman J.L., Verschueren K.H.G., Goldman A. The alpha/beta-hydrolase fold. Protein Eng. 1992;5:197–211. doi: 10.1093/protein/5.3.197. [DOI] [PubMed] [Google Scholar]
- 48.Campbell P.M., Newcomb R.D., Russell R.J., Oakeshott J.G. Two different amino acid substitutions in the aliesterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol. 1998;28:139–150. doi: 10.1016/S0965-1748(97)00109-4. [DOI] [Google Scholar]
- 49.Hartley C.J., Newcomb R.D., Russell R.J., Yong C.G., Stevens J.R., Yeates D.K., Salle J., Oakeshott J.G. Amplification of DNA from preserved specimens shows blowflies were predapted for the rapid evolution of insecticide resistance. Proc Natl Acad Sci USA. 2006;103:8757–8762. doi: 10.1073/pnas.0509590103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Heidari R., Devonshire A.L., Campbell B.E., Bell K.L., Dorrian S.J., Oakeshott J.G., Russell R.J. Hydrolysis of organophosphorus insecticides by in vitro modified carboxylesterase E3 from Lucilia cuprina. Insect Biochem Mol Biol. 2004;34:353–363. doi: 10.1016/j.ibmb.2004.01.001. [DOI] [PubMed] [Google Scholar]
- 51.Newcomb R.D., Campbell P.M., Ollis D.L., Cheah E., Russell R.J., Oakeshott J.G. A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc Natl Acad Sci USA. 1997;94:7464–7468. doi: 10.1073/pnas.94.14.7464. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Heidari R., Devonshire A.L., Campbell B.E., Dorrian S.J., Oakeshott J.G., Russell R.J. Hydrolysis of pyrethroids by carboxylesterases from Lucilia cuprina and Drosophila melanogaster with active sites modified by in vitro mutagenesis Insect. Biochem Mol Biol. 2005;35:597–609. doi: 10.1016/j.ibmb.2005.02.018. [DOI] [PubMed] [Google Scholar]
- 53.Heikinheimo P., Goldman A., Jeffries C., Ollis D.L. Of barn owls and bankers: a lush variety of alpha/beta hydrolases Struct. Fold Des. 1999;7:R141–R146. doi: 10.1016/S0969-2126(99)80079-3. [DOI] [PubMed] [Google Scholar]
- 54.Nardini M., Dijkstra B.W. Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol. 1999;9:732–737. doi: 10.1016/S0959-440X(99)00037-8. [DOI] [PubMed] [Google Scholar]
- 55.Bugg T.D.H. Diverse catalytic activities in the alpha beta-hydrolase family of enzymes: activation of H2O, HCN, H2O2, and O2. Bioorgan Chem. 2004;32:367–375. doi: 10.1016/j.bioorg.2004.05.005. [DOI] [PubMed] [Google Scholar]
- 56.Harcourt R.L., Horne I., Sutherland T.D., Hammock B.D., Russell R.J., Oakeshott J.G. Development of a simple and sensitive fluorimetric method for isolation of coumaphos-hydrolysing bacteria. Lett Appl Microbiol. 2002;34:263–268. doi: 10.1046/j.1472-765x.2002.01078.x. [DOI] [PubMed] [Google Scholar]
- 57.Serdar C.M., Gibson D.T., Munnecke D.M., Lancaster J.H. Enzymatic hydrolysis of organophosphates: cloning and expression of a parathion hydrolase gene from Pseudomonas diminuta. Biotechnol. 1985;3:367–371. doi: 10.1038/nbt0685-567. [DOI] [Google Scholar]
- 58.Mulbry W.W., Karns J.S., Kearney P.C., Nelson J.O., McDaniel C.S., Wild J.R. Identification of a plasmid-borne parathion hydrolase gene from Flavobacterium sp. by southern hybridization with opd from Pseudomonas diminuta. Appl Environ Microbiol. 1986;51:926–930. doi: 10.1128/aem.51.5.926-930.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Yang H., Carr P.D., McLoughlin S.Y., Liu J.W., Horne I., Qiu X., Jeffries C.M., Russell R.J., Oakeshott J.G., Ollis D.L. Evolution of an organophosphate-degrading enzyme: a comparison of natural and directed evolution. Protein Eng. 2003;16:135–145. doi: 10.1093/proeng/gzg013. [DOI] [PubMed] [Google Scholar]
- 60.Jackson C.J., Carr P.D., Kim H.K., Liu J.W., Herrald P., Mitic N., Schenk G., Smith C.A., Ollis D.L. Anomalous scattering analysis of Agrobacterium radiobacter phosphotriesterase: the prominent role of iron in the heterobinuclear active site. Biochem J. 2006;397:501–508. doi: 10.1042/BJ20060276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Jackson C., Kim H.K., Carr P.D., Liu J.W., Ollis D.L. The structure of an enzyme-product complex reveals the critical role of a terminal hydroxide nucleophile in the bacterial phosphotriesterase mechanism. Biochim Biophys Acta. 2005;1752:56–64. doi: 10.1016/j.bbapap.2005.06.008. [DOI] [PubMed] [Google Scholar]
- 62.Afriat L., Roodveldt C., Manco G., Tawfik D.S. The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase. Biochem. 2006;45:13677–13686. doi: 10.1021/bi061268r. [DOI] [PubMed] [Google Scholar]
- 63.Souza M.L., Sadowsky M.J., Wackett L.P. Atrazine chlorohydrolase from Pseudomonas sp. strain ADP: gene sequence, enzyme purification, and protein characterization. J Bacteriol. 1996;178:4894–4900. doi: 10.1128/jb.178.16.4894-4900.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Mulbry W.W., Zhu H., Nour S.M., Topp E. The triazine hydrolase gene trzN from Nocardioides sp. strain C190: cloning and construction of gene-specific primers. FEMS Microbiol Lett. 2002;206:75–79. doi: 10.1111/j.1574-6968.2002.tb10989.x. [DOI] [PubMed] [Google Scholar]
- 65.Lai K., Stolowich N.J., Wild J.R. Characterization of P-S bond hydrolysis in organophosphorothioate pesticides by organophosphorus hydrolase. Arch Biochem Biophys. 1995;318:59–64. doi: 10.1006/abbi.1995.1204. [DOI] [PubMed] [Google Scholar]
- 66.Dumas D.P., Durst H.D., Landis W.G., Raushel F.M., Wild J.R. Inactivation of organophosphorus nerve agents by the phosphotriesterase from Pseudomonas diminuta. Arch Biochem Biophys. 1990;277:155–159. doi: 10.1016/0003-9861(90)90564-F. [DOI] [PubMed] [Google Scholar]
- 67.Watkins L.M., Mahoney H.J., McCulloch J.K., Raushel F.M. Augmented hydrolysis of diisopropyl fluorophosphate in engineered mutants of phosphotriesterase. J Biol Chem. 1997;272:25596–25601. doi: 10.1074/jbc.272.41.25596. [DOI] [PubMed] [Google Scholar]
- 68.Raveh L., Segall Y., Leader H., Rothschild N., Levanon D., Henis Y., Ashani Y. Protection against tabun toxicity in mice by prophylaxis with an enzyme hydrolyzing organophosphate esters. Biochem Pharmacol. 1992;44:397–400. doi: 10.1016/0006-2952(92)90028-H. [DOI] [PubMed] [Google Scholar]
- 69.Roodveldt C., Tawfik D.S. Shared promiscuous activities and evolutionary features in various members of the amidohydrolase superfamily. Biochem. 2005;44:12728–12736. doi: 10.1021/bi051021e. [DOI] [PubMed] [Google Scholar]
- 70.Roodveldt C., Tawfik D.S. Directed evolution of phosphotriesterase from Pseudomonas diminuta for heterologous expression in Escherichia coli results in stabilization of the metal-free state. Protein Eng Des Sel. 2005;18:51–58. doi: 10.1093/protein/gzi005. [DOI] [PubMed] [Google Scholar]
- 71.Shim H., Hong S.B., Raushel F.M. Hydrolysis of phosphodiesters through transformation of the bacterial phosphotriesterase. J Biol Chem. 1998;273:17445–17450. doi: 10.1074/jbc.273.28.17445. [DOI] [PubMed] [Google Scholar]
- 72.Kutz F.W., Wood P.H., Bottimore D.P. Organochlorine pesticides and polychlorinated biphenyls in human adipose tissue. Rev Environ Contam Toxicol. 1991;120:1–82. doi: 10.1007/978-1-4612-3080-9_1. [DOI] [PubMed] [Google Scholar]
- 73.Nagata Y., Nariya T., Ohtomo R., Fukuda M., Yano K., Takagi M. Cloning and sequencing of a dehalogenase gene encoding an enzyme with hydrolase activity involved in the degradation of γ-hexachlorohexane in Pseudomonas paucimobilis. J Bacteriol. 1993;175:6403–6410. doi: 10.1128/jb.175.20.6403-6410.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74.Negri A, Marco E, Damborsky J and Gago F (2007) Stepwise dissection and visualization of the catalytic mechanism of haloalkane dehalogenase LinB using molecular dynamics simulations and computer graphics. J Mol Graph Model [Epub ahead of print] [DOI] [PubMed]
- 75.Nagata Y., Prokop Z., Sato Y., Jerabek P., Kumar A., Ohtsubo Y., Tsuda M., Damborsky J. Degradation of β-hexachlorcyclohexane by haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26. Appl Environ Microbiol. 2005;71:2183–2185. doi: 10.1128/AEM.71.4.2183-2185.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76.Sharma P., Raina V., Kumari R., Shweta M., Dogra C., Kumari H., Kohler H.P.E., Holliger C., Lal R. Haloalkane dehalogenase LinB is responsible for β-and δ-hexachlorocyclohexane transformation in Sphingobium indicum B90A. Appl Environ Microbiol. 2006;72:5720–5727. doi: 10.1128/AEM.00192-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77.Ito M, Prokop Z, Klvana M, Otsubo Y, Tsuda M, Damborsky J and Nagata Y (2007) Degradation of β-hexachlorocyclohexane by haloalkane dehalogenase LinB from γ-hexachlorocyclohexane-utalizing bacterium Sphingobium MI1205. Arch Microbiol [Epub ahead of print] [DOI] [PubMed]
- 78.Prokop Z., Moninvoca M., Chaloupkova R., Klvana M., Nagata Y., Janssen D.B., Damborsky Catalytic mechanism of the haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26. J Biol Chem. 2003;278:45094–45100. doi: 10.1074/jbc.M307056200. [DOI] [PubMed] [Google Scholar]
- 79.Mandelbaum R.T., Allan D.L., Wackett L.P. Isolation and characterization of a Pseudomonas sp. that mineralizes the S-triazine herbicide atrazine. Appl Environ Microbiol. 1995;61:1451–1457. doi: 10.1128/aem.61.4.1451-1457.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Seffernick J.L., Souza M.L., Sadowsky M.J., Wackett L.P. Melamine deaminase and atrazine chlorohydrolase: 98 percent identical but functionally different. J Bacteriol. 2001;183:2405–2410. doi: 10.1128/JB.183.8.2405-2410.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81.Mulbry W.W., Zhu H., Nour S.M., Topp E. The triazine hydrolase gene trzN from Nocardioides sp. strain C190: cloning and construction of gene-specific primers. FEMS Microbiol Lett. 2002;206:75–79. doi: 10.1111/j.1574-6968.2002.tb10989.x. [DOI] [PubMed] [Google Scholar]
- 82.Strong L.C., Rosendahl C., Johnson G., Andreina M., Sadowsky M.J., Wackett L.P. Arthrobacter aurescens TC1 metabolises diverse s-triazine ring compounds. Appl Environ Microbiol. 2002;68:5973–5980. doi: 10.1128/AEM.68.12.5973-5980.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 83.Shapir N., Pederson C., Gil O., Strong L., Seffernick J., Sadowsky M.J., Wackett L.P. TrzN from Arthrobacter aurescens TC1 is a zinc amidohydrolase. J bacteriol. 2006;188:5859–5864. doi: 10.1128/JB.00517-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Shapir N., Johnson G., Andreina M., Sadowsky M.J., Wackett L.P. Substrate specificity and colorimetric assay for recombinant TrzN derived from Arthrobacter aurescens TC1. Appl Environ Microbiol. 2005;71:2214–2220. doi: 10.1128/AEM.71.5.2214-2220.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 85.Wang L., Samac D.A., Shapir N., Wackett L.P., Vance C.P., Olszewskiand N.E., Sadowsky M.J. Biodegradation of atrazine in transgenic plants expressing a modified bacterial atrazine chlorohydrolase (atzA) gene. Plnt Biotechnol J. 2005;3:475–486. doi: 10.1111/j.1467-7652.2005.00138.x. [DOI] [PubMed] [Google Scholar]
- 86.Sawers G. Biochemistry, physiology and molecular biology of glycyl radical enzymes. FEMS Microbiol Rev. 1998;22:543–551. doi: 10.1111/j.1574-6976.1998.tb00386.x. [DOI] [Google Scholar]
- 87.Nagata Y., Imai R., Sakai A., Fukuda M., Yano K., Takagi M. Isolation and characterisation of Tn5-induced mutants of Pseudomonas paucimobilis UT26 defective in γ-hexachlorocyclohexane dehydrochlorinase (LinA) Biosci Biotechnol Biochem. 1993;57:703–709. doi: 10.1271/bbb.57.703. [DOI] [PubMed] [Google Scholar]
- 88.Nagata Y., Mori K., Takagi M., Murzin A.G., Damborsky J. Identification of protein fold and catalytic residues of γ-hexachlorocyclohexane dehydrochlorinase LinA. Proteins. 2001;45:471–477. doi: 10.1002/prot.10007. [DOI] [PubMed] [Google Scholar]
- 89.Trantirek L., Hybkova K., Nagata Y., Murzin A., Ansorgova A., Sklenar V., Damborsky J. Reaction mechanism and sterochemistry of γ-hexachlorocyclohexane dehydrochlorinase LinA. J Biol Chem. 2001;276:7734–7740. doi: 10.1074/jbc.M007452200. [DOI] [PubMed] [Google Scholar]
- 90.Raina V, Suar M, Singh A, Prakash O, Dadhwal M, Gupta SK, Dogra C, Lawlor K, Lal S, van der Meer JR, Holliger C and Lal R (2007) Enhanced biodegradation of hexachlorocyclohexane (HCH) in contaminated soils via inoculation with Sphingobium indicum B90A. Biodegradation. [Epub ahead of print] [DOI] [PubMed]
- 91.Rice G.C., Goeddel D.V., Cachianes G., Woronicz J., Chen E.Y., Williams S.R., Leung D.W. Random PCR mutagenesis screening of secreted proteins by direct expression in mammalian cells. Proc Natl Acad Sci USA. 1992;89:5467–5471. doi: 10.1073/pnas.89.12.5467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92.Stemmer W.P.C. Rapid evolution of a protein in vitro by DNA shuffling. Nature. 1994;370:389–391. doi: 10.1038/370389a0. [DOI] [PubMed] [Google Scholar]
- 93.Ostermeier M., Nixon A.E., Shim J.H., Benkovic S.J. Combinatorial protein engineering by incremental truncation. Proc. Natl. Acad Sci USA. 1999;96:3562–3567. doi: 10.1073/pnas.96.7.3562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 94.Lutz S., Ostermeier M., Moore G.L., Maranas C.D., Benkovic Creating multiple-crossover DNA libraries independent of sequence identity. Proc Natl Acad Sci USA. 2001;98:11248–11253. doi: 10.1073/pnas.201413698. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 95.Herman A., Tawfik D.S. Incorporating Synthetic Oligonucleotides via Gene Reassembly (ISOR): a versatile tool for generating targeted libraries. Protein Eng Des Sel. 2007;20:219–226. doi: 10.1093/protein/gzm014. [DOI] [PubMed] [Google Scholar]
- 96.Reetz M.T., Bocola M., Carballeira J.D., Zha D., Vogel A. Expanding the range of substrate acceptance of enzymes: combinatorial active-site saturation test. Angew Chem. 2005;117:4264–4268. doi: 10.1002/ange.200500767. [DOI] [PubMed] [Google Scholar]
- 97.Raillard S., Krebber A., Chen Y., Ness J.E., Bermudez E., Trinidad R., Fullem R., Davis C., Welch M., Seffernick J., Wackett L.P., Stemmer W.P.C., Minshull J. Novel enzyme activities and functional plasticity revealed by recombining highly homologous enzymes. Chem Biol. 2001;8:891–898. doi: 10.1016/S1074-5521(01)00061-8. [DOI] [PubMed] [Google Scholar]
- 98.Mencia M., Martinex-Ferri A.I., Alcalde M., Lorenzo V. Identification of a γ-hexachlorocyclohexane dehydrochlorinase (LinA) variant with improved expression and solubility properties. Biocatal Biotrans. 2006;24:223–230. doi: 10.1080/10242420600667809. [DOI] [Google Scholar]
- 99.Cho C.M., Mulchadnani A., Chen W. Bacterial cell surface display of organophosphorus hydrolase for selective screening of improved hydrolysis of organophosphate nerve agents. Appl Environ Microbiol. 2002;68:2026–2030. doi: 10.1128/AEM.68.4.2026-2030.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 100.Cho C.M., Mulchadnani A., Chen W. Altering the substrate specificity of organophosphorus hydrolase for enhanced hydrolysis of chlorpyrifos. Appl Environ Microbiol. 2004;70:4681–4685. doi: 10.1128/AEM.70.8.4681-4685.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 101.McLoughlin S.Y., Jackson C., Liu J.W., Ollis D.L. Increased expression of a bacterial phosphotriesterase in Escherichia coli through directed evolution. Protein Expr Purif. 2005;41:433–440. doi: 10.1016/j.pep.2005.01.012. [DOI] [PubMed] [Google Scholar]
- 102.Behrens M.A., Mutlu N., Chakraborty S., Dumitru R., Jiang W.Z., LaVallee B.J., Herman P.L., Clemente T.E., Weeks D.P. Dicamba resistance: enlarging and preserving biotechnology-based weed management strategies. Science. 2007;316:1185–1188. doi: 10.1126/science.1141596. [DOI] [PubMed] [Google Scholar]
- 103.Herman P.L., Behrens M., Chakraborty S., Chrastil B.M., Barycki J., Weeks D.P. A Three-component Dicamba O-Demethylase from Pseudomonas maltophilia, Strain DI-6. J Biol Chem. 2005;26:24759–24767. doi: 10.1074/jbc.M500597200. [DOI] [PubMed] [Google Scholar]
- 104.Wright T, Lira JM, Walsh TA, Merlo DJ, Jayakumar PS and Lin G. Novel herbicide resistance genes. Patent 2007 WO 2007/053482 A2