A selection assay for haloalkane dehalogenase activity based on toxic substrates

Applied Microbiology and Biotechnology

Volumn 99, Issue 21, 2015, Pages 8955-8962

  Fibinger, Michael P C ^a   Davids, Timo ^b   Böttcher, Dominique ^a   Bornscheuer, Uwe T ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b Davids Biotechnologie GmbH   (Germany)

Author keywords

Continuous selection process; Growth assay; Haloalkane dehalogenase; Toxicity

Indexed keywords

LIBRARIES; TOXICITY;

ARTIFICIAL SUBSTRATES; CONTINUOUS SELECTION; DEHALOGENASE; DIRECTED EVOLUTION; HALOGENATED ALKANES; HIGH THROUGHPUT SYSTEMS; NATURAL SELECTION; SURVIVAL-OF-THE-FITTEST;

ENZYMES;

ALKANE; ENZYME VARIANT; HALOALKANE DEHALOGENASE; HYDROLASE; TOXIC SUBSTANCE; UNCLASSIFIED DRUG; ALKENE; HALOGENATED HYDROCARBON; MUTANT PROTEIN;

ALKANE; ASSAY; BIOTECHNOLOGY; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; FITNESS; HALOCARBON; HYDROLYSIS; NATURAL SELECTION; SUBSTRATE; SURVIVAL; TOXICITY;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON SOURCE; COMBINATORIAL LIBRARY; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GROWTH CURVE; HYDROLYSIS; NATURAL SELECTION; NONHUMAN; PLASMID; SITE DIRECTED MUTAGENESIS; TOXICITY TESTING; BIOASSAY; GENETIC SCREENING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROCEDURES;

ALKENES; BIOLOGICAL ASSAY; ESCHERICHIA COLI; GENETIC TESTING; HYDROCARBONS, HALOGENATED; HYDROLASES; MUTANT PROTEINS;

EID: 84945461959     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6686-y     Document Type: Article

References (46)

1. Acevedo-Rocha CG, Agudo R, Reetz MT (2014) Directed evolution of stereoselective enzymes based on genetic selection as opposed to screening systems. J Biotechnol 191:3–10
2. Altenbuchner J (1988) A new E.coli cloning vector containing a melanin marker for insertion screening. Nucleic Acids Res 16(17):8710
3. Archer IVJ (1997) Epoxide hydrolases as asymmetric catalysts. Tetrahedron 53(46):15617–15662
4. Arnold FH (1998) Design by directed evolution. Acc Chem Res 31(3):125–131
5. Arnold FH, Volkov AA (1999) Directed evolution of biocatalysts. Curr Opin Chem Biol 3(1):54–59
6. Bahl CD, Morisseau C, Bomberger JM, Stanton BA, Hammock BD, O’Toole GA, Madden DR (2010) Crystal structure of the cystic fibrosis transmembrane conductance regulator inhibitory factor Cif reveals novel active-site features of an epoxide hydrolase virulence factor. J Bacteriol 192(7):1785–1795
7. Bornscheuer UT (2013) Protein engineering as a tool for the development of novel bioproduction systems. Adv Biochem Eng Biotechnol 137:25–40
8. Bornscheuer UT, Pohl M (2001) Improved biocatalysts by directed evolution and rational protein design. Curr Opin Chem Biol 5(2):137–143
9. Bornscheuer UT, Huisman GW, Kazlauskas RJ, Lutz S, Moore JC, Robins K (2012) Engineering the third wave of biocatalysis. Nature 485(7397):185–194
10. Bosma T, Damborsky J, Stucki G, Janssen DB (2002) Biodegradation of 1,2,3-trichloropropane through directed evolution and heterologous expression of a haloalkane dehalogenase gene. Appl Environ Microbiol 68(7):3582–3587
11. Böttcher D, Schmidt M, Bornscheuer UT (2008) Alteration of substrate specificity and stereoselectivity of lipases and esterases protein engineering handbook. Wiley-VCH Verlag GmbH & Co. KGaA, pp 753–775
12. Chaloupkova R, Sykorova J, Prokop Z, Jesenska A, Monincovaa M, Pavlova M, Tsuda M, Nagata Y, Damborsky J (2003) Modification of activity and specificity of haloalkane dehalogenase from Sphingomonas paucimobilis UT26 by engineering of its entrance tunnel. J Biol Chem 278(52):52622–52628
13. Chen K, Arnold FH (1993) Tuning the activity of an enzyme for unusual environments: sequential random mutagenesis of subtilisin E for catalysis in dimethylformamide. Proc Natl Acad Sci 90(12):5618–5622
14. Chovancova E, Kosinski J, Bujnicki JM, Damborsky J (2007) Phylogenetic analysis of haloalkane dehalogenases. Proteins 67(2):305–316
15. Christians FC, Loeb LA (1996) Novel human DNA alkyltransferases obtained by random substitution and genetic selection in bacteria. Proc Natl Acad Sci 93(12):6124–6128
16. Dvorak P, Bidmanova S, Damborsky J, Prokop Z (2014) Immobilized synthetic pathway for biodegradation of toxic recalcitrant pollutant 1,2,3-trichloropropane. Environ Sci Technol 48(12):6859–6866
17. Fernández-Álvaro E, Snajdrova R, Jochens H, Davids T, Böttcher D, Bornscheuer UT (2011) A combination of in vivo selection and cell sorting for the identification of enantioselective biocatalysts. Angew Chem 50:8584–8587
18. Fetzner S, Lingens F (1994) Bacterial dehalogenases: biochemistry, genetics, and biotechnological applications. Microbiol Rev 58(4):641–685
19. Gribble GW (2010) Naturally occurring organohalogen compounds: a comprehensive update. Springer, Wien
20. Holloway P, Trevors JT, Lee H (1997) A colorimetric assay for detecting haloalkane dehalogenase activity. J Microbiol Methods 32(1):31–36
21. Janssen DB (2004) Evolving haloalkane dehalogenases. Curr Opin Chem Biol 8(2):150–159
22. Janssen DB, Pries F, Vanderploeg J, Kazemier B, Terpstra P, Witholt B (1989) Cloning of 1,2-dichloroethane degradation genes of Xanthobacter autotrophicus GJ10 and expression and sequencing of the dhla gene. J Bacteriol 171(12):6791–6799
23. Janssen DB, Oppentocht JE, Poelarends GJ (2001) Microbial dehalogenation. Curr Opin Biotechnol 12(3):254–258
24. Jesenska A, Pavlova M, Strouhal M, Chaloupkova R, Tesinska I, Monincova M, Prokop Z, Bartos M, Pavlik I, Rychlik I, Mobius P, Nagata Y, Damborsky J (2005) Cloning, biochemical properties, and distribution of mycobacterial haloalkane dehalogenases. Appl Environ Microbiol 71(11):6736–6745
25. Jochens H, Hesseler M, Stiba K, Padhi SK, Kazlauskas RJ, Bornscheuer UT (2011) Protein engineering of alpha/beta-hydrolase fold enzymes. ChemBioChem 12(10):1508–1517
26. Kawasaki H, Kuriyama H, Tonomura K (1995) Use of haloacetate dehalogenase genes as selection markers for Escherichia coli and Pseudomonas vectors. Biodegradation 6(3):213–216
27. Kazlauskas R (2009) Engineering enantioselectivity in enzyme-catalyzed reactions. In: Lutz S, Bornscheuer UT (eds) Protein engineering handbook. Wiley-VCH, Weinheim, pp 15–47
28. Keuning S, Janssen DB, Witholt B (1985) Purification and characterization of hydrolytic haloalkane dehalogenase from Xanthobacter autotrophicus GJ10. J Bacteriol 163(2):635–639
29. Koudelakova T, Chovancova E, Brezovsky J, Monincova M, Fortova A, Jarkovsky J, Damborsky J (2011) Substrate specificity of haloalkane dehalogenases. Biochem J 435(2):345–354
30. Koudelakova T, Bidmanova S, Dvorak P, Pavelka A, Chaloupkova R, Prokop Z, Damborsky J (2013) Haloalkane dehalogenases: biotechnological applications. Biotechnol J 8(1):32–45
31. Kulakova AN, Larkin MJ, Kulakov LA (1997) The plasmid-located haloalkane dehalogenase gene from Rhodococcus rhodochrous NCIMB 13064. Microbiology 143(Pt 1):109–115
32. MacBeath G, Kast P, Hilvert D (1998) Redesigning enzyme topology by directed evolution. Science 279(5358):1958–1961
33. Miyazaki K (2003) Creating random mutagenesis libraries by megaprimer PCR of whole plasmid (MEGAWHOP). Methods Mol Biol 231:23–28
34. Nardini M, Ridder IS, Rozeboom HJ, Kalk KH, Rink R, Janssen DB, Dijkstra BW (1999) The X-ray structure of epoxide hydrolase from Agrobacterium radiobacter AD1 - An enzyme to detoxify harmful epoxides. J Biol Chem 274(21):14579–14586
35. Newman J, Peat TS, Richard R, Kan L, Swanson PE, Affholter JA, Holmes IH, Schindler JF, Unkefer CJ, Terwilliger TC (1999) Haloalkane dehalogenases: structure of a Rhodococcus enzyme. Biochemistry 38(49):16105–16114
36. Pavlova M, Klvana M, Prokop Z, Chaloupkova R, Banas P, Otyepka M, Wade RC, Tsuda M, Nagata Y, Damborsky J (2009) Redesigning dehalogenase access tunnels as a strategy for degrading an anthropogenic substrate. Nat Chem Biol 5(10):727–733
37. Prokop Z, Sato Y, Brezovsky J, Mozga T, Chaloupkova R, Koudelakova T, Jerabek P, Stepankova V, Natsume R, van Leeuwen JG, Janssen DB, Florian J, Nagata Y, Senda T, Damborsky J (2010) Enantioselectivity of haloalkane dehalogenases and its modulation by surface loop engineering. Angew Chem Int Ed Engl 49(35):6111–6115
38. Reetz MT, Hobenreich H, Soni P, Fernandez L (2008) A genetic selection system for evolving enantioselectivity of enzymes. Chem Commun 43:5502–5504
39. Roth JR, Kugelberg E, Reams AB, Kofoid E, Andersson DI (2006) Origin of mutations under selection: the adaptive mutation controversy. Annu Rev Microbiol 60:477–501
40. Schmidt-Dannert C, Arnold FH (1999) Directed evolution of industrial enzymes. Trends Biotechnol 17(4):135–136
41. Steele DF, Jinks-Robertson S (1992) An examination of adaptive reversion in Saccharomyces cerevisiae. Genetics 132(1):9–21
42. Stepankova V, Bidmanova S, Koudelakova T, Prokop Z, Chaloupkova R, Damborsky J (2013) Strategies for stabilization of enzymes in organic solvents. ACS Catal 3(12):2823–2836
43. Swaving J, de Bont JAM (1998) Microbial transformation of epoxides. Enzym Microb Technol 22(1):19–26
44. Tang LX, van Merode AEJ, Spelberg JHL, Fraaije MW, Janssen DB (2003) Steady-state kinetics and tryptophan fluorescence properties of halohydrin dehalogenase from Agrobacterium radiobacter. Roles of W139 and W249 in the active site and halide-induced conformational change. Biochemistry 42(47):14057–14065
45. van Leeuwen JG, Wijma HJ, Floor RJ, van der Laan JM, Janssen DB (2012) Directed evolution strategies for enantiocomplementary haloalkane dehalogenases: from chemical waste to enantiopure building blocks. ChemBioChem 13(1):137–148
46. Yano T, Oue S, Kagamiyama H (1998) Directed evolution of an aspartate aminotransferase with new substrate specificities. Proc Natl Acad Sci 95(10):5511–5515