Synthesis of chiral 2-alkanols from n-alkanes by a P. putida whole-cell biocatalyst

Biotechnology and Bioengineering

Volumn 113, Issue 9, 2016, Pages 1845-1852

  Tieves, Florian ^a   Erenburg, Isabelle N ^a   Mahmoud, Osama ^a   Urlacher, Vlada B ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

2 octanol; ADH; alkanes; CYP154A8; P. putida; P450

Indexed keywords

BACTERIA; BIOCATALYSTS; CELLS; CYTOLOGY; ENZYMES; ESCHERICHIA COLI;

2-OCTANOL; ALCOHOL DEHYDROGENASE; CYP154A8; P. PUTIDA; P450; PSEUDOMONAS PUTIDA; RECOMBINANT ESCHERICHIA COLI; WHOLE CELL BIOCATALYSTS;

PARAFFINS;

ALCOHOL DEHYDROGENASE; ALKANE DERIVATIVE; ALKANOL; CYTOCHROME P450; CYTOCHROME P450 154A8; HEPTANE; METHYL BETA CYCLODEXTRIN; NONANE; OCTANE; UNCLASSIFIED DRUG;

ARTICLE; BIOCATALYST; BIOTRANSFORMATION; CHIRALITY; ENERGY RESOURCE; ESCHERICHIA COLI; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PSEUDOMONAS PUTIDA; SYNTHESIS;

EID: 84979752421     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25953     Document Type: Article

References (65)

1. Bar R. 1989. Cyclodextrin-aided bioconversions and fermentations. Trends Biotechnol 7:2–4.
2. Bayer T, Milker S, Wiesinger T, Rudroff F, Mihovilovic MD. 2015. Designer microorganisms for optimized redox cascade reactions—Challenges and future perspectives. Adv Synth Catal 357:1587–1618.
3. Bernhardt R, Urlacher VB. 2014. Cytochromes P450 as promising catalysts for biotechnological application: Chances and limitations. Appl Microbiol Biotechnol 98:6185–6203.
4. Blank LM, Ebert BE, Buehler K, Bühler B. 2010. Redox biocatalysis and metabolism: Molecular mechanisms and metabolic network analysis. Antioxid Redox Signal 13:349–394.
5. Blank LM, Ionidis G, Ebert BE, Bühler B, Schmid A. 2008. Metabolic response of Pseudomonas putida during redox biocatalysis in the presence of a second octanol phase. FEBS J 275:5173–5190.
6. Bracco P, Janssen DB, Schallmey A. 2013. Selective steroid oxyfunctionalisation by CYP154C5, a bacterial cytochrome P450. Microb Cell Fact 12:95.
7. Bühler B, Park J, Blank LM, Schmid A. 2008. NADH availability limits asymmetric biocatalytic epoxidation in a growing recombinant Escherichia coli strain. Appl Environ Microbiol 74:1436–1446.
8. Choi K, Kumar A, Schweizer HP. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: Application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64:391–397.
9. Choi K, Park H, Kim B. 2010. Characterization of bi-functional CYP154 from Nocardia farcinica IFM10152 in the O-dealkylation and ortho-hydroxylation of formononetin. Enzyme Microb Technol 47:327–334.
10. Craft DL, Madduri KM, Eshoo M, Wilson CR. 2003. Identification and characterization of the CYP52 family of Candida tropicalis ATCC 20336, important for the conversion of fatty acids and alkanes to α,ω-dicarboxylic acids. Appl Environ Microbiol 69:5983–5991.
11. de Carvalho CCCR, Da Cruz AARL, Pons M, Pinheiro HMRV, Cabral JMS, Da Fonseca MMR, Ferreira BS, Fernandes P. 2004. Mycobacterium sp., Rhodococcus erythropolis, and Pseudomonas putida behavior in the presence of organic solvents. Microsc Res Tech 64:215–222.
12. Fujii T, Narikawa T, Sumisa F, Arisawa A, Takeda K, Kato J. 2006. Production of α, ω-alkanediols using Escherichia coli expressing a cytochrome P450 from Acinetobacter sp. OC4. Biosci Biotechnol Biochem 70:1379–1385.
13. Fujita N, Sumisa F, Shindo K, Kabumoto H, Arisawa A, Ikenaga H, Misawa N. 2009. Comparison of two vectors for functional expression of a bacterial cytochrome P450 gene in Escherichia coli using CYP153 genes. Biosci Biotechnol Biochem 73:1825–1830.
14. Funhoff EG, Bauer U, García-Rubio I, Witholt B, van Beilen JB. 2006. CYP153A6, a soluble P450 oxygenase catalyzing terminal-alkane hydroxylation. J Bacteriol 188:5220–5227.
15. Gaur R, Khare SK. 2009. Cellular response mechanisms in Pseudomonas aeruginosa PseA during growth in organic solvents. Lett Appl Microbiol 49:372–377.
16. Gibson DG, Young L, Chuang R, Venter JC, Hutchison CA, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343–345.
17. Glieder A, Farinas ET, Arnold FH. 2002. Laboratory evolution of a soluble, self-sufficient, highly active alkane hydroxylase. Nat Biotechnol 20:1135–1139.
18. Goldberg K, Schroer K, Lütz S, Liese A. 2007a. Biocatalytic ketone reduction—A powerful tool for the production of chiral alcohols—Part I: Processes with isolated enzymes. Appl Microbiol Biotechnol 76:237–248.
19. Goldberg K, Schroer K, Lütz S, Liese A. 2007b. Biocatalytic ketone reduction—A powerful tool for the production of chiral alcohols—Part II: Whole-cell reductions. Appl Microbiol Biotechnol 76:249–255.
20. Grant C, Deszcz D, Wei Y, Martínez-Torres RJ, Morris P, Folliard T, Sreenivasan R, Ward J, Dalby P, Woodley JM, Baganz F. 2014. Identification and use of an alkane transporter plug-in for applications in biocatalysis and whole-cell biosensing of alkanes. Sci Rep 4:5844.
21. 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 48:480–486.
22. Gudiminchi RK, Randall C, Opperman DJ, Olaofe OA, Harrison STL, Albertyn J, Smit MS. 2012. Whole-cell hydroxylation of n-octane by Escherichia coli strains expressing the CYP153A6 operon. Appl Microbiol Biotechnol 96:1507–1516.
23. Hannemann F, Bichet A, Ewen KM, Bernhardt R. 2007. Cytochrome P450 systems-biological variations of electron transport chains. Biochim Biophys Acta 1770:330–344.
24. He Y, Tao Z, Ding Y, Zhang D, Wu Y, Lu Y, Liu F, Xue Y, Wang C, Xu J. 2015. Effective biosynthesis of ethyl (R)-4-chloro-3-hydroxybutanoate by supplementation of L-glutamine, D-xylose and β-cyclodextrin in n-butyl acetate-water media. J Biotechnol 203:62–67.
25. Heipieper HJ, Neumann G, Cornelissen S, Meinhardt F. 2007. Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 74:961–973.
26. Hummel W. 1997. New alcohol dehydrogenases for the synthesis of chiral compounds. Adv Biochem Eng Biotechnol 58:145–184.
27. BAD is in Pseudomonas putida KT2440 independent of Crp-cAMP activation. Appl Microbiol Biotechnol 85:1923–1933.
28. Julsing MK, Schrewe M, Cornelissen S, Hermann I, Schmid A, Bühler B. 2012. Outer membrane protein AlkL boosts biocatalytic oxyfunctionalization of hydrophobic substrates in Escherichia coli. Appl Environ Microbiol 78:5724–5733.
29. 3 to calcitriol using Pseudonocardia sp. KCTC 1029BP. Bioprocess Biosyst Eng 38:1281–1290.
30. Kell DB, Swainston N, Pir P, Oliver SG. 2015. Membrane transporter engineering in industrial biotechnology and whole cell biocatalysis. Trends Biotechnol 33:237–246.
31. Koch DJ, Chen MM, van Beilen JB, Arnold FH. 2009. In vivo evolution of butane oxidation by terminal alkane hydroxylases AlkB and CYP153A6. Appl Environ Microbiol 75:337–344.
32. Kubota M, Nodate M, Yasumoto-Hirose M, Uchiyama T, Kagami O, Shizuri Y, Misawa N. 2005. Isolation and functional analysis of cytochrome P450 CYP153A genes from various environments. Biosci Biotechnol Biochem 69:2421–2430.
33. Ladkau N, Schmid A, Bühler B. 2014. The microbial cell-functional unit for energy dependent multistep biocatalysis. Curr Opin Biotechnol 30:178–189.
34. Leuchs S, Greiner L. 2011. Alcohol dehydrogenase from Lactobacillus brevis: A versatile robust catalyst for enantioselective transformations. Chem Biochem Eng Q 2:267–281.
35. Lewis JC, Coelho PS, Arnold FH. 2011. Enzymatic functionalization of carbon-hydrogen bonds. Chem Soc Rev 40:2003–2021.
36. 2-tolerant hydrogenase and a P450 monooxygenase. Chem Commun (Camb) 51:16173–16175.
37. Lundemo MT, Notonier S, Striedner G, Hauer B, Woodley JM. 2016. Process limitations of a whole-cell P450 catalyzed reaction using a CYP153A-CPR fusion construct expressed in Escherichia coli. Appl Microbiol Biotechnol 100:1197–1208.
38. Meinhold P, Peters MW, Hartwick A, Hernandez AR, Arnold FH. 2006. Engineering cytochrome P450 BM3 for terminal alkane hydroxylation. Adv Synth Catal 348:763–772.
39. Mi J, Becher D, Lubuta P, Dany S, Tusch K, Schewe H, Buchhaupt M, Schrader J. 2014. De novo production of the monoterpenoid geranic acid by metabolically engineered Pseudomonas putida. Microb Cell Fact 13(1):170.
40. Mouri T, Michizoe J, Ichinose H, Kamiya N, Goto M. 2006. A recombinant Escherichia coli whole cell biocatalyst harboring a cytochrome P450cam monooxygenase system coupled with enzymatic cofactor regeneration. Appl Microbiol Biotechnol 72:514–520.
41. Nodate M, Kubota M, Misawa N. 2006. Functional expression system for cytochrome P450 genes using the reductase domain of self-sufficient P450RhF from Rhodococcus sp. NCIMB 9784. Appl Microbiol Biotechnol 71:455–462.
42. Nolte JC, Urlacher VB. Oxidation via C-H activation. Cytochrome P450 in the oxidation of alkanes. In: Faber K, Fessner W, Turner N, editors. Science of synthesis: Biocatalysis in organic synthesis. Stuttgart: Georg Thieme. p 21–64.
43. Olaofe OA, Fenner CJ, Gudiminchi RK, Smit MS, Harrison STL. 2013. The influence of microbial physiology on biocatalyst activity and efficiency in the terminal hydroxylation of n-octane using Escherichia coli expressing the alkane hydroxylase, CYP153A6. Microb Cell Fact 12:8.
44. Omura T, Sato R. 1964. The carbon monoxide-binding pigment of liver microsomes. II. solubilization, purification and properties. J Biol Chem 239:2379–2385.
45. O'Reilly E, Köhler V, Flitsch SL, Turner NJ. 2011. Cytochromes P450 as useful biocatalysts: Addressing the limitations. Chem Commun (Camb) 47:2490–2501.
46. Pennec A, Jacobs CL, Opperman DJ, Smit MS. 2015. Revisiting cytochrome P450-mediated oxyfunctionalization of linear and cyclic alkanes. Adv Synth Catal 357:118–130.
47. Peters MW, Meinhold P, Glieder A, Arnold FH. 2003. Regio- and enantioselective alkane hydroxylation with engineered cytochromes P450 BM-3. J Am Chem Soc 125:13442–13450.
48. Poblete-Castro I, Becker J, Dohnt K, dos Santos VM, Wittmann C. 2012. Industrial biotechnology of Pseudomonas putida and related species. Appl Microbiol Biotechnol 93:2279–2290.
49. Ramos J, Sol Cuenca M, Molina-Santiago C, Segura A, Duque E, Gómez-García MR, Udaondo Z, Roca A. 2015. Mechanisms of solvent resistance mediated by interplay of cellular factors in Pseudomonas putida. FEMS Microbiol Rev 39:555–566.
50. Roduner E, Kaim W, Sarkar B, Urlacher VB, Pleiss J, Gläser R, Einicke W, Sprenger GA, Beifuß U, Klemm E, Liebner C, Hieronymus H, Hsu S, Plietker B, Laschat S. 2013. Selective catalytic oxidation of C-H bonds with molecular oxygen. ChemCatChem 5:82–112.
51. Roiban G, Reetz MT. 2015. Expanding the toolbox of organic chemists: Directed evolution of P450 monooxygenases as catalysts in regio- and stereoselective oxidative hydroxylation. Chem Commun (Camb) 51:2208–2224.
52. Scheps D, Malca SH, Hoffmann H, Nestl BM, Hauer B. 2011. Regioselective ω-hydroxylation of medium-chain n-alkanes and primary alcohols by CYP153 enzymes from Mycobacterium marinum and Polaromonas sp. strain JS666. Org Biomol Chem 9:6727–6733.
53. Schewe H, Holtmann D, Schrader J. 2009. P450 BM-3-catalyzed whole-cell biotransformation of alpha-pinene with recombinant Escherichia coli in an aqueous-organic two-phase system. Appl Microbiol Biotechnol 83:849–857.
54. Schrewe M, Julsing MK, Bühler B, Schmid A. 2013. Whole-cell biocatalysis for selective and productive C-O functional group introduction and modification. Chem Soc Rev 42:6346–6377.
55. Segura A, Molina L, Fillet S, Krell T, Bernal P, Muñoz-Rojas J, Ramos J. 2012. Solvent tolerance in Gram-negative bacteria. Curr Opin Biotechnol 23:415–421.
56. Sevrioukova IF, Poulos TL. 2011. Structural biology of redox partner interactions in P450cam monooxygenase: A fresh look at an old system. Arch Biochem Biophys 507:66–74.
57. Singh M, Sharma R, Banerjee UC. 2002. Biotechnological applications of cyclodextrins. Biotechnol Adv 20:341–359.
58. Vallon T, Glemser M, Malca SH, Scheps D, Schmid J, Siemann-Herzberg M, Hauer B, Takors R. 2013. Production of 1-Octanol from n-Octane by Pseudomonas putida KT2440. Chem Ing Tech 85:841–848.
59. van Beilen JB, Funhoff EG. 2005. Expanding the alkane oxygenase toolbox: New enzymes and applications. Curr Opin Biotechnol 16:308–314.
60. van Beilen JB, Funhoff EG. 2007. Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21.
61. von Bühler C, Le-Huu P, Urlacher VB. 2013. Cluster screening: An effective approach for probing the substrate space of uncharacterized cytochrome P450s. Chembiochem 14:2189–2198.
62. von Bühler CJ, Urlacher VB. 2014. A novel P450-based biocatalyst for the selective production of chiral 2-alkanols. Chem Commun (Camb) 50:4089–4091.
63. Weber E, Seifert A, Antonovici M, Geinitz C, Pleiss J, Urlacher VB. 2011. Screening of a minimal enriched P450 BM3 mutant library for hydroxylation of cyclic and acyclic alkanes. Chem Commun (Camb) 47:944–946.
64. Willrodt C, Karande R, Schmid A, Julsing MK. 2015. Guiding efficient microbial synthesis of non-natural chemicals by physicochemical properties of reactants. Curr Opin Biotechnol 35:52–62.
65. Yang Y, Liu J, Li Z. 2014. Engineering of P450pyr hydroxylase for the highly regio- and enantioselective subterminal hydroxylation of alkanes. Angew Chem Int Ed Engl 126:3184–3188.