Switching a newly discovered lactonase into an efficient and thermostable phosphotriesterase by simple double mutations His250Ile/Ile263Trp

Biotechnology and Bioengineering

Volumn 111, Issue 10, 2014, Pages 1920-1930

  Luo, Xiao Jing ^a   Kong, Xu Dong ^a   Zhao, Jian ^a   Chen, Qi ^a   Zhou, Jiahai ^b   Xu, Jian He ^a  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

Author keywords

Functional switch; Lactonase; Organophosphate; Phosphotriesterase; Site directed mutagenesis; X ray crystallography

Indexed keywords

BACTERIA; DETOXIFICATION; ESTERS; X RAY CRYSTALLOGRAPHY;

CATALYTIC EFFICIENCIES; ESTERASE ACTIVITIES; LACTONASE; ORGANOPHOSPHATE; PHOSPHOTRIESTERASES; SITE DIRECTED MUTAGENESIS; SUBSTRATE RECOGNITION; SYNTHETIC CHEMICALS;

HYDROLASES;

ARYLDIALKYLPHOSPHATASE; BACTERIAL ENZYME; ESTERASE; GLUCONOLACTONASE; PARATHION METHYL; PHOSPHOTRIESTERASE; BETA LACTAMASE;

ARTICLE; CRYSTAL STRUCTURE; DETOXIFICATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME STABILITY; MOLECULAR DOCKING; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PSEUDOMONAS OLEOVORANS; PSEUDOMONAS PUTIDA; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

PSEUDOMONAS OLEOVORANS; PSEUDOMONAS PUTIDA;

AMINO ACID SEQUENCE; ARYLDIALKYLPHOSPHATASE; BETA-LACTAMASES; CRYSTALLOGRAPHY, X-RAY; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORIC TRIESTER HYDROLASES; PROTEIN CONFORMATION; PROTEIN STABILITY; PSEUDOMONAS OLEOVORANS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 84906784355     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25272     Document Type: Article

References (61)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(2):213-221.
2. Afriat L, Roodveldt C, Manco G, Tawfik DS. 2006. The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase. Biochemistry 45(46):13677-13686.
3. Afriat-Jurnou L, Jackson CJ, Tawfik DS. 2012. Reconstructing a missing link in the evolution of a recently diverged phosphotriesterase by active-site loop remodeling. Biochemistry 51(31):6047-6055.
4. Aharoni A, Gaidukov L, Khersonsky O, Gould SM, Roodveldt C, Tawfik DS. 2004. The 'evolvability' of promiscuous protein functions. Nat Genet 37(1):73-76.
5. Amitai G, Gaidukov L, Adani R, Yishay S, Yacov G, Kushnir M, Teitlboim S, Lindenbaum M, Bel P, Khersonsky O, Tawfik DS, Meshulam H. 2006. Enhanced stereoselective hydrolysis of toxic organophosphates by directly evolved variants of mammalian serum paraoxonase. FEBS J 273(9):1906-1919.
6. Aubert SD, Li Y, Raushel FM. 2004. Mechanism for the hydrolysis of organophosphates by the bacterial phosphotriesterase. Biochemistry 43(19):5707-5715.
7. Bar-Rogovsky H, Hugenmatter A, Tawfik DS. 2013. The evolutionary origins of detoxifying enzymes: The mammalian serum paraoxonases (PONs) relate to bacterial homoserine lactonases. J Biol Chem 288(33):23914-23927.
8. Ben-David M, Elias M, Filippi JJ, Duñach E, Silman I, Sussman JL, Tawfik DS. 2012. Catalytic versatility and backups in enzyme active sites: The case of serum paraoxonase 1. J Mol Biol 418(3):181-196.
9. Briseño-Roa L, Timperley CM, Griffiths AD, Fersht AR. 2011. Phosphotriesterase variants with high methylphosphonatase activity and strong negative trade-off against phosphotriesters. Protein Eng Des Sel 24(1-2):151-159.
10. Chu XY, Wu NF, Deng MJ, Tian J, Yao B, Fan YL. 2006. Expression of organophosphorus hydrolase OPHC2 in Pichia pastoris: Purification and characterization. Protein Expr Purif 49(1):9-14.
11. Cui ZL, Li SP, Fu GP. 2001. Isolation of methyl parathion-degrading strain M6 and cloning of the methyl parathion hydrolase gene. Appl Environ Microbiol 67(10):4922-4925.
12. Dong YJ, Bartlam M, Sun L, Zhou YF, Zhang ZP, Zhang CG, Rao Z, Zhang XE. 2005. Crystal structure of methyl parathion hydrolase from Pseudomonas sp. WBC-3. J Mol Biol 353(3):655-663.
13. Draganov DI, La Du BN. 2004. Pharmacogenetics of paraoxonases: A brief review. Naunyn Schmiedebergs Arch Pharmacol 369(1):78-88.
14. Dumas DP, Caldwell SR, Wild JR, Raushel FM. 1989. Purification and properties of the phosphotriesterase from Pseudomonas diminuta. J Biol Chem 264(33):19659-19665.
15. Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
16. Ekkhunnatham A, Jongsareejit B, Yamkunthong W, Wichitwechkarn J. 2012. Purification and characterization of methyl parathion hydrolase from Burkholderia cepacia capable of degrading organophosphate insecticides. World J Microbiol Biotechnol 28(4):1739-1746.
17. Elias M, Dupuy J, Merone L, Mandrich L, Porzio E, Moniot S, Rochu D, Lecomte C, Rossi M, Masson P, Manco G, Chabriere E. 2008. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J Mol Biol 379(5):1017-1028.
18. Elias M, Tawfik DS. 2012. Divergence and convergence in enzyme evolution: Parallel evolution of paraoxonases from quorum-quenching lactonases. J Biol Chem 287(1):11-20.
19. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(12):2126-2132.
20. Ghanem E, Raushel FM. 2005. Detoxification of organophosphate nerve agents by bacterial phosphotriesterase. Toxicol Appl Pharmacol 207(2):459-470.
21. Gotthard G, Hiblot J, Gonzalez D, Chabriere E, Elias M. 2012. Crystallization and preliminary X-ray diffraction analysis of the organophosphorus hydrolase OPHC2 from Pseudomonas pseudoalcaligenes. Acta Crystallogr Sect F Struct Biol Cryst Commun 69(1):73-76.
22. Gotthard G, Hiblot J, Gonzalez D, Elias M, Chabriere E. 2013. Structural and enzymatic characterization of the phosphotriesterase OPHC2 from Pseudomonas pseudoalcaligenes. PLoS ONE 8(11):e77995.
23. Hawwa R, Larsen SD, Ratia K, Mesecar AD. 2009. Structure-based and random mutagenesis approaches increase the organophosphate-degrading activity of a phosphotriesterase homologue from Deinococcus radiodurans. J Mol Biol 393(1):36-57.
24. Hiblot J, Gotthard G, Chabriere E, Elias M. 2012. Structural and enzymatic characterization of the lactonase SisLac from Sulfolobus islandicus. PLoS ONE 7(10):e47028.
25. Khersonsky O, Roodveldt C, Tawfik DS. 2006. Enzyme promiscuity: Evolutionary and mechanistic aspects. Curr Opin Chem Biol 10(5):498-508.
26. Khersonsky O, Tawfik DS. 2005. Structure-reactivity studies of serum paraoxonase PON1 suggest that its native activity is lactonase. Biochemistry 44(16):6371-6382.
27. Khersonsky O, Tawfik DS. 2006. The histidine 115-histidine 134 dyad mediates the lactonase activity of mammalian serum paraoxonases. J Biol Chem 281(11):7649-7656.
28. Khersonsky O, Tawfik DS. 2010. Enzyme promiscuity: A mechanistic and evolutionary perspective. Annu Rev Biochem 79:471-505.
29. Kim MH, Choi WC, Kang HO, Lee JS, Kang BS, Kim KJ, Derewenda ZS, Oh TK, Lee CH, Lee JK. 2005. The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-L-homoserine lactone hydrolase. Proc Natl Acad Sci USA 102(49):17606-17611.
30. Li X, He J, Li S. 2007. Isolation of a chlorpyrifos-degrading bacterium, Sphingomonas sp. strain Dsp-2, and cloning of the mpd gene. Res Microbiol 158(2):143-149.
31. Liu D, Momb J, Thomas PW, Moulin A, Petsko GA, Fast W, Ringe D. 2008. Mechanism of the quorum-quenching lactonase (AiiA) from Bacillus thuringiensis. 1. Product-bound structures. Biochemistry 47(29):7706-7714.
32. Liu H, Zhang JJ, Wang SJ, Zhang XE, Zhou NY. 2005. Plasmid-borne catabolism of methyl parathion and p-nitrophenol in Pseudomonas sp. strain WBC-3. Biochem Biophys Res Commun 334(4):1107-1114.
33. Luo XJ, Yu HL, Xu JH. 2012. Genomic data mining: An efficient way to find new and better enzymes. Enzyme Eng 1:104. doi: 10.4172/eeg.1000104
34. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40(4):658-674.
35. Meier MM, Rajendran C, Malisi C, Fox NG, Xu C, Schlee S, Barondeau DP, Raushel FM. 2013. Molecular engineering of organophosphate hydrolysis activity from a weak promiscuous lactonase template. J Am Chem Soc 135(31):11670-11677.
36. Merone L, Mandrich L, Porzio E, Rossi M, Müller S, Reiter G, Worek F, Manco G. 2010. Improving the promiscuous nerve agent hydrolase activity of a thermostable archaeal lactonase. Bioresour Technol 101(23):9204-9212.
37. Merone L, Mandrich L, Rossi M, Manco G. 2005. A thermostable phosphotriesterase from the archaeon Sulfolobus solfataricus: Cloning, overexpression and properties. Extremophiles 9(4):297-305.
38. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 30(16):2785-2791.
39. Munnecke DM. 1976. Enzymatic hydrolysis of organophosphate insecticides, a possible pesticide disposal method. Appl Environ Microbiol 32(1):7-13.
40. Omburo GA, Kuo JM, Mullins LS, Raushel FM. 1992. Characterization of the zinc binding site of bacterial phosphotriesterase. J Biol Chem 267(19):13278-13283.
41. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data. Methods Enzymol 276:307-326.
42. Parthasarathy S, Murthy MRN. 2000. Protein thermal stability: Insights from atomic displacement parameters (B values). Protein Eng 13(1):9-13.
43. Porzio E, Merone L, Mandrich L, Rossi M, Manco G. 2007. A new phosphotriesterase from Sulfolobus acidocaldarius and its comparison with the homologue from Sulfolobus solfataricus. Biochimie 89(5):625-636.
44. Qian L, Liu JY, Liu JY, Yu HL, Li CX, Xu JH. 2011. Fingerprint lipolytic enzymes with chromogenic p-nitrophenyl esters of structurally diverse carboxylic acids. J Mol Catal B Enzym 73(1):22-26.
45. Qiu XH, Bai WQ, Zhong QZ, Li M, He FQ, Li BT. 2006. Isolation and characterization of a bacterial strain of the genus Ochrobactrum with methyl parathion mineralizing activity. J Appl Microbiol 101(5):986-994.
46. Raushel FM. 2002. Bacterial detoxification of organophosphate nerve agents. Curr Opin Microbiol 5(3):288-295.
47. Roodveldt C, Tawfik DS. 2005. Shared promiscuous activities and evolutionary features in various members of the amidohydrolase superfamily. Biochemistry 44(38):12728-12736.
48. Shen YJ, Lu P, Mei H, Yu HJ, Hong Q, Li SP. 2010. Isolation of a methyl parathion-degrading strain Stenotrophomonas sp. SMSP-1 and cloning of the ophc2 gene. Biodegradation 21(5):785-792.
49. Singh BK. 2008. Organophosphorus-degrading bacteria: Ecology and industrial applications. Nat Rev Microbiol 7(2):156-164.
50. Singh BK, Walker A. 2006. Microbial degradation of organophosphorus compounds. FEMS Microbiol Rev 30(3):428-471.
51. Theriot CM, Grunden AM. 2011. Hydrolysis of organophosphorus compounds by microbial enzymes. Appl Microbiol Biotechnol 89(1):35-43.
52. Tian J, Wang P, Huang L, Chu X, Wu N, Fan Y. 2013. Improving the thermostability of methyl parathion hydrolase from Ochrobactrum sp. M231 using a computationally aided method. Appl Microbiol Biotechnol 97(7):2997-3006.
53. Tokuriki N, Stricher F, Serrano L, Tawfik DS. 2008. How protein stability and new functions trade off. PLoS Comput Biol 4(2):e1000002.
54. Tokuriki N, Tawfik DS. 2009. Stability effects of mutations and protein evolvability. Curr Opin Struct Biol 19:596-604.
55. Wu NF, Deng MJ, Liang GY, Chu XY, Yao B, Fan YL. 2004. Cloning and expression of ophc2, a new organophosphorus hydrolase gene. Chin Sci Bull 49(12):1245-1249.
56. Xiang DF, Kolb P, Fedorov AA, Meier MM, Fedorov LV, Nguyen TT, Sterner R, Almo SC, Shoichet BK, Raushel FM. 2009. Functional annotation and three-dimensional structure of Dr0930 from Deinococcus radiodurans, a close relative of phosphotriesterase in the amidohydrolase superfamily. Biochemistry 48(10):2237-2247.
57. Yeung DT, Lenz DE, Cerasoli DM. 2005. Analysis of active-site amino-acid residues of human serum paraoxonase using competitive substrates. FEBS J 272(9):2225-2230.
58. Zhang Y, An J, Ye W, Yang G, Qian ZG, Chen HF, Cui L, Feng Y. 2012. Enhancing the promiscuous phosphotriesterase activity of a thermostable lactonase (GkaP) for the efficient degradation of organophosphate pesticides. Appl Environ Microbiol 78(18):6647-6655.
59. Zhang Z, Hong Q, Xu J, Zhang X, Li S. 2006. Isolation of fenitrothion-degrading strain Burkholderia sp. FDS-1 and cloning of mpd gene. Biodegradation 17(3):275-283.
60. Zheng B, Yu S, Zhang Y, Feng Y, Lou Z. 2011. Crystallization and preliminary crystallographic analysis of the phosphotriesterase-like lactonase from Geobacillus kaustophilus. Acta Crystallogr Sect F Struct Biol Cryst Commun 67(7):794-796.
61. Zheng L, Baumann U, Reymond JL. 2004. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res 32:e115.