Directed evolution of nitrobenzene dioxygenase for the synthesis of the antioxidant hydroxytyrosol

Applied Microbiology and Biotechnology

Volumn 98, Issue 11, 2014, Pages 4975-4985

  Bernath Levin, Kalia ^a   Shainsky, Janna ^a   Sigawi, Liron ^a   Fishman, Ayelet ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Family shuffling; Hydroxytyrosol; Neutral drift; Nitrobenzene dioxygenase; Protein engineering

Indexed keywords

ANTIOXIDANTS; BIOCHEMICAL ENGINEERING; DETOXIFICATION; GENETIC ENGINEERING; HYDROGEN BONDS; LIBRARIES; SUBSTRATES;

DIOXYGENASES; FAMILY SHUFFLING; HYDROXYTYROSOL; NEUTRAL DRIFT; PROTEIN ENGINEERING;

NITROBENZENE;

DIOXYGENASE; HYDROXYTYROSOL; NITROBENZENE; 3,4-DIHYDROXYPHENYLETHANOL; ANTIOXIDANT; MUTANT PROTEIN; NITROBENZENE DERIVATIVE; PHENETHYL ALCOHOL;

ANTIOXIDANT; CHEMICAL BONDING; DRUG; ENZYME ACTIVITY; MOLECULAR ANALYSIS; MUTATION; OXYGEN; PROTEIN; SUBSTRATE;

ARTICLE; BACTERIAL MUTATION; BACTERIAL STRAIN; CONTROLLED STUDY; DETOXIFICATION; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME SYNTHESIS; GENE LIBRARY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROGEN BOND; INDUSTRIAL WASTE; MASS FRAGMENTOGRAPHY; NONHUMAN; PROTEIN ENGINEERING; PROTON NUCLEAR MAGNETIC RESONANCE; THIN LAYER CHROMATOGRAPHY; AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; DIRECTED MOLECULAR EVOLUTION; GENETICS; KINETICS; METABOLISM; MISSENSE MUTATION; STRUCTURE ACTIVITY RELATION;

AMINO ACID SUBSTITUTION; ANTIOXIDANTS; DIOXYGENASES; DIRECTED MOLECULAR EVOLUTION; KINETICS; MUTANT PROTEINS; MUTATION, MISSENSE; NITROBENZENES; PHENYLETHYL ALCOHOL; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84901687222     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5505-6     Document Type: Article

References (53)

1. Allouche N, Sayadi S (2005) Synthesis of hydroxytyrosol, 2-hydroxyphenylacetic acid, and 3-hydroxyphenylacetic acid by differential conversion of tyrosol isomers using Serratia marcescens strain. J Agric Food Chem 53(16):6525-6530 (Pubitemid 41169408)
2. Allouche N, Fki I, Sayadi S (2003) Toward a high yield recovery of antioxidants and purified hydroxytyrosol from olive mill wastewaters. J Agric Food Chem 52(2):267-273
3. Allouche N, Damak M, Ellouz R, Sayadi S (2004) Use of whole cells of Pseudomonas aeruginosa for synthesis of the antioxidant hydroxytyrosol via conversion of tyrosol. Appl Environ Microbiol 70(4):2105-2109 (Pubitemid 38500509)
4. Amitai G, Gupta RD, Tawfik DS (2007) Latent evolutionary potentials under the neutral mutational drift of an enzyme. HFSP J 1(1):67-78
5. Bloom JD, Labthavikul ST, Otey CR, Arnold FH (2006) Protein stability promotes evolvability. Proc Natl Acad Sci U S A 103(15):5869-5874
6. Bouallagui Z, Bouaziz M, Lassoued S, Engasser JM, Ghoul M, Sayadi S (2011) Hydroxytyrosol acyl esters: biosynthesis and activities. Appl Biochem Biotechnol 163(5):592-599
7. Boyd DR, Sharma ND, Allen CC (2001) Aromatic dioxygenases: molecular biocatalysis and applications. Curr Opin Biotechnol 12(6):564-573 (Pubitemid 34146507)
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgramquantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
9. Brouk M, Fishman A (2009) Protein engineering of toluene monooxygenases for synthesis of hydroxytyrosol. Food Chem 116:114-121
10. Brouk M, Fishman A (2012) Improving process conditions of hydroxytyrosol synthesis by toluene-4-monooxygenase. J Mol Catal B Enzym 84:121-127
11. Brouk M, Nov Y, Fishman A (2010) Improving biocatalyst performance by integrating statistical methods into protein engineering. Appl Environ Microbiol 76(19):6397-6403
12. Carredano E, Karlsson A, Kauppi B, Choudhury D, Parales RE, Parales JV, Lee K, Gibson DT, Eklund H, Ramaswamy S (2000) Substrate binding site of naphthalene 1,2-dioxygenase: functional implications of indole binding. J Mol Biol 296(2):701-712
13. Cicerale S, Lucas L, Keast R (2012) Antimicrobial, antioxidant and anti-inflammatory phenolic activities in extra virgin olive oil. Curr Opin Biotechnol 23(2):129-135
14. Dalby PA (2011) Strategy and success for the directed evolution of enzymes. Curr Opin Struct Biol 21(4):473-480
15. Dror A, Fishman A (2012) Engineering non-heme mono- and dioxygenases for biocatalysis. Comput Struct Biotechnol J 2(3):1-12
16. Espin JC, Soler-Rivas C, Cantos E, Tomas-Barberan FA, Wichers HJ (2001) Synthesis of the antioxidant hydroxytyrosol using tyrosinase as biocatalyst. J Agric Food Chem 49(3):1187-1193 (Pubitemid 32884931)
17. Feingersch R, Shainsky J, Wood TK, Fishman A (2008) Protein engineering of toluene monooxygenases for synthesis of chiral sulfoxides. Appl Environ Microbiol 74(5):1555-1566 (Pubitemid 351358453)
18. Ferraro DJ, Okerlund AL, Mowers JC, Ramaswamy S (2006) Structural basis for regioselectivity and stereoselectivity of product formation by naphthalene 1,2-dioxygenase. J Bacteriol 188(19):6986-6994 (Pubitemid 44497911)
19. Fishman A, Tao Y, Bentley WE, Wood TK (2004) Protein engineering of toluene 4-monooxygenase of Pseudomonas mendocina KR1 for synthesizing 4-nitrocatechol from nitrobenzene. Biotechnol Bioeng 87(6):779-790 (Pubitemid 39264647)
20. Friemann R, Ivkovic-Jensen MM, Lessner DJ, Yu CL, Gibson DT, Parales RE, Eklund H, Ramaswamy S (2005) Structural insight into the dioxygenation of nitroarene compounds: the crystal structure of nitrobenzene dioxygenase. J Mol Biol 348(5):1139-1151 (Pubitemid 40602372)
21. Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds - from one strategy to four. Nat Rev Microbiol 9(11):803-816
22. Grant C, Woodley JM, Baganz F (2011) Whole-cell bio-oxidation of n-dodecane using the alkane hydroxylase system of P. putida GPo1 expressed in E. coli. Enzyme Microb Technol 48(6-7):480-486
23. Gupta RD, Tawfik DS (2008) Directed enzyme evolution via small and effective neutral drift libraries. Nat Methods 5(11):939-942
24. Herman A, Tawfik DS (2007) Incorporating synthetic oligonucleotides via gene reassembly (ISOR): a versatile tool for generating targeted libraries. Protein Eng Des Sel 20(5):219-226 (Pubitemid 351321303)
25. Iyer LM, Aravind L, Koonin EV (2001a) Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 75(23):11720-11734 (Pubitemid 33063263)
26. Iyer LM, Koonin EV, Aravind L (2001b) Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily. Proteins 43(2):134-144
27. Ju KS, Parales RE (2006) Control of substrate specificity by active-site residues in nitrobenzene dioxygenase. Appl Environ Microbiol 72(3):1817-1824
28. Ju KS, Parales RE (2009) Application of nitroarene dioxygenases in the design of novel strains that degrade chloronitrobenzenes. Microb Biotechnol 2(2):241-252
29. Ju KS, Parales RE (2011) Evolution of a new bacterial pathway for 4-nitrotoluene degradation. Mol Microbiol 82(2):1365-2958
30. Kauppi B, Lee K, Carredano E, Parales RE, Gibson DT, Eklund H, Ramaswamy S (1998) Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure 6(5):571-586
31. Kovaleva EG, Lipscomb JD (2008) Versatility of biological non-heme Fe(II) centers in oxygen activation reactions. Nat Chem Biol 4(3):186-193 (Pubitemid 351265327)
32. Lessner DJ, Johnson GR, Parales RE, Spain JC, Gibson DT (2002) Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765. Appl Environ Microbiol 68(2):634-641 (Pubitemid 34113051)
33. Lipscomb JD (2008) Mechanism of extradiol aromatic ring-cleaving dioxygenases. Curr Opin Struct Biol 18(6):644-649
34. Mahajabeen P, Chadha A (2011) One-pot synthesis of enantiomerically pure 1, 2-diols: asymmetric reduction of aromatic α-oxoaldehydes catalysed by Candida parapsilosis ATCC 7330. Tetrahedron Asymmetry 22(24):2156-2160
35. 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
36. Nishino SF, Spain JC (1995) Oxidative pathway for the biodegradation of nitrobenzene by Comamonas sp. strain JS765. Appl Environ Microbiol 61(6):2308-2313
37. Parales RE (2003) The role of active-site residues in naphthalene dioxygenase. J Ind Microbiol Biotechnol 30(5):271-278
38. Parales RE, Huang R, Yu CL, Parales JV, Lee FK, Lessner DJ, Ivkovic-Jensen MM, Liu W, Friemann R, Ramaswamy S, Gibson DT (2005) Purification, characterization, and crystallization of the components of the nitrobenzene and 2-nitrotoluene dioxygenase enzyme systems. Appl Environ Microbiol 71(7):3806-3814 (Pubitemid 40980550)
39. Pavelka A, Chovancova E, Damborsky J (2009) HotSpotWizard: a web server for identification of hot spots in protein engineering. Nucleic Acids Res 37(Web Server issue):376-383
40. Reetz MT, Kahakeaw D, Lohmer R (2008) Addressing the numbers problem in directed evolution. Chembiochem 9(11):1797-1804
41. Resnick SM, Torok DS, Lee K, Brand JM, Gibson DT (1995) Regiospecific and stereoselective hydroxylation of 1-indanone and 2-indanone by naphthalene dioxygenase and toluene dioxygenase. Appl Environ Microbiol 61(2):847
42. Resnick SM, Lee K, Gibson DT (1996) Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Ind Microbiol Biotechnol 17(5):438-457
43. Sambrook J, Fritsch E,Maniatis T (1989) Molecular cloning: a laboratory manual, vol 2, 2nd edn. Cold Spring Harbor, NY
44. Satoh Y, Tajima K, Munekata M, Keasling JD, Lee TS (2012) Engineering of l-tyrosine oxidation in Escherichia coli and microbial production of hydroxytyrosol. Metab Eng 14(6):603-610
45. Schmidt M, Bornscheuer UT (2005) High-throughput assays for lipases and esterases. Biomol Eng 22(1-3):51-56 (Pubitemid 40602593)
46. Seo J, Kang SI, Ryu JY, Lee YJ, Park KD, Kim M,Won D, Park HY, Ahn JH, Chong Y, Kanaly RA, Han J, Hur HG (2010) Location of flavone B-ring controls regioselectivity and stereoselectivity of naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816-4. Appl Microbiol Biotechnol 86(5):1451-1462
47. Shainsky J, Bernath-Levin K, Isaschar-Ovdat S, Glaser F, Fishman A (2013) Protein engineering of nirobenzene dioxygenase for enantioselective synthesis of chiral sulfoxides. Protein Eng Des Sel 26(5):335-345
48. Stemmer WP (1994) DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc Natl Acad Sci U S A 91(22):10747-10751
49. Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455-461
50. Vargas RR, Bechara EJH, Marzorati L, Wladislaw B (1999) Asymmetric sulfoxidation of a beta-carbonyl sulfide series by chloroperoxidase. Tetrahedron Asymmetry 10(16):3219-3227 (Pubitemid 29481238)
51. Wackett LP (2002)Mechanism and applications of Rieske non-heme iron dioxygenases. Enzyme Microb Technol 31:577-587
52. Wei ZL, Lin GQ, Li ZY (2000) Microbial transformation of 2-hydroxy and 2-acetoxy ketones with Geotrichum sp. BioorgMed Chem 8(5):1129-1137
53. Yu CL, Parales RE, Gibson DT (2001) Multiple mutations at the active site of naphthalene dioxygenase affect regioselectivity and enantioselectivity. J Ind Microbiol Biotechnol 27(2):94-103 (Pubitemid 33702309)