Engineering of LadA for enhanced hexadecane oxidation using random- and site-directed mutagenesis

Applied Microbiology and Biotechnology

Volumn 94, Issue 4, 2012, Pages 1019-1029

  Dong, Yanpeng ^a,b   Yan, Jiang ^a,b   Du, Huiqian ^a,b   Chen, Miao ^a,b   Ma, Ting ^a,c   Feng, Lu ^a,b,c  

^a NANKAI UNIVERSITY   (China)

^b TEDA   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

Directed evolution; Error prone PCR; Hexadecane; Hydroxylase; LadA; Monooxygenase; Saturation site directed mutagenesis

Indexed keywords

DIRECTED EVOLUTION; ERROR PRONE PCR; HEXADECANE; HYDROXYLASES; LADA; MONOOXYGENASES; SITE DIRECTED MUTAGENESIS;

DEGRADATION; HYDROXYLATION; PARAFFINS; PH EFFECTS;

ENZYME ACTIVITY;

HEXADECANE; LADA PROTEIN; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

BACTERIUM; BIODEGRADATION; ENZYME ACTIVITY; GENE EXPRESSION; MUTAGENICITY; MUTATION; OXIDATION; REACTION KINETICS;

ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROXYLATION; IN VITRO STUDY; IN VIVO STUDY; MUTAGENESIS; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PH; PROTEIN EXPRESSION; PSEUDOMONAS FLUORESCENS; RANDOM DIRECTED MUTAGENESIS; SITE DIRECTED MUTAGENESIS; THERMOSTABILITY;

ALKANES; ENZYME STABILITY; GENETIC COMPLEMENTATION TEST; GEOBACILLUS; HYDROGEN-ION CONCENTRATION; KINETICS; METABOLIC ENGINEERING; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; MUTAGENESIS; MUTANT PROTEINS; MUTATION, MISSENSE; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PSEUDOMONAS FLUORESCENS; TEMPERATURE;

GEOBACILLUS THERMODENITRIFICANS; PSEUDOMONAS FLUORESCENS;

EID: 84862833975     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4035-y     Document Type: Article

References (44)

1. Arnold FH, Moore JC (1997) Optimizing industrial enzymes by directed evolution. Adv Biochem Eng Biotechnol 58:1-14
2. Banner DW, Bloomer AC, Petsko GA, Phillips DC, Pogson CI, Wilson IA, Corran PH, Furth AJ,Milman JD, Offord RE, Priddle JDWaley SG (1975) Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 angstrom resolution using amino acid sequence data. Nature 255(5510):609-614
3. Bernstein FC, Koetzle TF,Williams GJ, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) The Protein Data Bank. A computer-based archival file for macromolecular structures. Eur J Biochem 80(2):319-324
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
5. Brakstad OG, Lodeng AG (2005) Microbial diversity during biodegradation of crude oil in seawater from the North Sea. Microb Ecol 49(1):94-103
6. Domanski TL, Halpert JR (2001) Analysis of mammalian cytochrome P450 structure and function by site-directed mutagenesis. Curr Drug Metab 2(2):117-137
7. Dubbels BL, Sayavedra-Soto LA, Arp DJ (2007) Butane monooxygenase of 'Pseudomonas butanovora': purification and biochemical characterization of a terminal-alkane hydroxylating diiron monooxygenase. Microbiology 153(6):1808-1816
8. Farinas ET, Arnold FH (2001) Directed enzyme evolution. Curr Opin Biotechnol 12(6):545-551
9. Fasan R, Chen MM, Crook NC, Arnold FH (2007) Engineered alkane-hydroxylating cytochrome P450BM3 exhibiting nativelike catalytic properties. Angew Chem Int Ed Engl 46 (44):8414-8418
10. Feng L, Wang W, Cheng J, Ren Y, Zhao G, Gao C, Tang Y, Liu X, Han W, Peng X, Liu R,Wang L (2007) Genome and proteome of longchain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc Natl Acad Sci U S A 104(13):5602-5607
11. Grant MA (2009) Protein structure prediction in structure-based ligand design and virtual screening. Comb Chem High Throughput Screen 12(10):940-960
12. Guex N, Peitsch MC, Schwede T (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30(Suppl 1):S162-S173
13. Gutteridge A, Thornton J (2005) Conformational changes observed in enzyme crystal structures upon substrate binding. J Mol Biol 346 (1):21-28
14. Harayama S, Kasai Y, Hara A (2004) Microbial communities in oilcontaminated seawater. Curr Opin Biotechnol 15(3):205-214
15. Honma W, LiW, Liu H, Scott EE, Halpert JR (2005) Functional role of residues in the helix B'region of cytochrome P450 2B1. Arch Biochem Biophys 435(1):157-165
16. Javadpour MM, Eilers M, Groesbeek M, Smith SO (1999) Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys J 77(3):1609-1618
17. Joo H, Lin Z, Arnold FH (1999) Laboratory evolution of peroxidemediated cytochrome P450 hydroxylation. Nature 399 (6737):670-673
18. Kotani T, Yamamoto T, Yurimoto H, Sakai Y, Kato N (2003) Propane monooxygenase and NAD+-dependent secondary alcohol dehydrogenase in propane metabolism by Gordonia sp. strain TY-5. J Bacteriol 185(24):7120-7128
19. Kumar S, Scott EE, Liu H, Halpert JR (2003) A rational approach to re-engineer cytochrome P450 2B1 regioselectivity based on the crystal structure of cytochrome P450 2 C5. J Biol Chem 278 (19):17178-17184
20. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680-685
21. Leisola M, Turunen O (2007) Protein engineering: opportunities and challenges. Appl Microbiol Biotechnol 75(6):1225-1232
22. Lentz OA, Feenstra A, Habicher T, Hauer B, Schmid RD, Urlacher VB (2006) Altering the regioselectivity of cytochrome P450 CYP102A3 of Bacillus subtilis by using a new versatile assay system. ChemBioChem 7(2):345-350
23. Li L, Liu X, YangW, Xu F,WangW, Feng L, Bartlam M,Wang L, Rao Z (2008) Crystal structure of long-chain alkane monooxygenase (LadA) in complex with coenzyme FMN: unveiling the longchain alkane hydroxylase. J Mol Biol 376(2):453-465
24. Li W, Liu H, Scott EE, Grater F, Halpert JR, Luo X, Shen J, Jiang H (2005) Possible pathway(s) of testosterone egress from the active site of cytochrome P450 2B1: a steered molecular dynamics simulation. Drug Metab Dispos 33(7):910-919
25. Liu X, Dong Y, Zhang J, Zhang A, Wang L, Feng L (2009) Two novel metal-independent long-chain alkyl alcohol dehydrogenases from Geobacillus thermodenitrificans NG80-2. Microbiology 155(Pt 6):2078-2085
26. Marchant R, Sharkey FH, Banat IM, Rahman TJ, Perfumo A (2006) The degradation of n-hexadecane in soil by thermophilic geobacilli. FEMS Microbiol Ecol 56(1):44-54
27. Moonen JH, Marco W, Fraaije IMCM, Rietjens CL, van Berkel JH (2002) Flavoenzyme-catalyzed oxygenations and oxidations of phenolic compounds. Adv Synth Catal 344(10):1023-1035
28. McDonald IR, Miguez CB, Rogge G, Bourque D, Wendlandt KD, Groleau D, Murrell JC (2006) Diversity of soluble methane monooxygenase-containing methanotrophs isolated from polluted environments. FEMS Microbiol Lett 255(2):225-232
29. Olson AJ, Goodsell DS (1998) Automated docking and the search for HIV protease inhibitors. SAR QSAR Environ Res 8(3-4):273-285
30. Rui L, Kwon YM, Fishman A, Reardon KF, Wood TK (2004) Saturation mutagenesis of toluene ortho-monooxygenase of Burkholderia cepacia G4 for enhanced 1-naphthol synthesis and chloroform degradation. Appl Environ Microbiol 70(6):3246-3252
31. Scott EE, Halpert JR (2005) Structures of cytochrome P450 3A4. Trends Biochem Sci 30(1):5-7
32. Scott EE, He YA, Wester MR, White MA, Chin CC, Halpert JR, Johnson EF, Stout CD (2003) An open conformation of mammalian cytochrome P450 2B4 at 1.6-Å resolution. Proc Natl Acad Sci U S A 100(23):13196-13201
33. Scott EE, He YQ, Halpert JR (2002) Substrate routes to the buried active site may vary among cytochromes P450: mutagenesis of the F-G region in P450 2B1. Chem Res Toxicol 15(11):1407-1413
34. Scott EE, Liu H, Qun He Y, LiW, Halpert JR (2004a) Mutagenesis and molecular dynamics suggest structural and functional roles for residues in the N-terminal portion of the cytochrome P450 2B1 I helix. Arch Biochem Biophys 423(2):266-276
35. Scott EE, White MA, He YA, Johnson EF, Stout CD, Halpert JR (2004b) Structure of mammalian cytochrome P450 2B4 complexed with 4-(4-chlorophenyl) imidazole at 1.9-Å resolution: insight into the range of P450 conformations and the coordination of redox partner binding. J Biol Chem 279(26):27294-27301
36. Smits TH, Balada SB, Witholt B, van Beilen JB (2002) Functional analysis of alkane hydroxylases from gram-negative and grampositive bacteria. J Bacteriol 184(6):1733-1742
37. Smits TH, Seeger MA, Witholt B, van Beilen JB (2001) New alkaneresponsive expression vectors for Escherichia coli and Pseudomonas. Plasmid 46(1):16-24
38. Szklarz GD, Halpert JR (1997a) Molecular modeling of cytochrome P450 3A4. J Comput Aided Mol Des 11(3):265-272
39. Szklarz GD, Halpert JR (1997b) Use of homology modeling in conjunction with site-directed mutagenesis for analysis of structure-function relationships of mammalian cytochromes P450. Life Sci 61(26):2507-2520
40. Tsotsou GE, Cass AE, Gilardi G (2002) High throughput assay for cytochrome P450 BM3 for screening libraries of substrates and combinatorial mutants. Biosens Bioelectron 17(1-2):119-131
41. Tulchin NL, Ornstein L, Davis BJ (1976) A microgel system for disc electrophoresis. Anal Biochem 72:485-490
42. van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74 (1):13-21
43. van Beilen JB, Funhoff EG, van Loon A, Just A, Kaysser L, Bouza M, Holtackers R, Rothlisberger M, Li Z, Witholt B (2006) Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl Environ Microbiol 72(1):59-65
44. van Beilen JB, Wubbolts MG, Witholt B (1994) Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5(3-4):161-174