Efficient hydroxylation of 1,8-cineole with monoterpenoid-resistant recombinant Pseudomonas putida GS1

World Journal of Microbiology and Biotechnology

Volumn 32, Issue 7, 2016, Pages

  Mi, Jia ^a   Schewe, Hendrik ^a   Buchhaupt, Markus ^a   Holtmann, Dirk ^a   Schrader, Jens ^a  

^a DECHEMA FORSCHUNGSINSTITUT   (Germany)

Author keywords

1,8 Cineole; Biotransformation; Hydroxylation; Monoterpene; P450cin; Pseudomonas putida; Whole cell biocatalysis

Indexed keywords

BIOCATALYSTS; BIOCONVERSION; CELLS; CYTOLOGY; ESCHERICHIA COLI; MONOTERPENES; UNSATURATED COMPOUNDS;

1 ,8-CINEOLE; BIOTRANSFORMATION; MONOTERPENE; P450CIN; PSEUDOMONAS PUTIDA; WHOLE-CELL BIOCATALYSIS;

HYDROXYLATION;

CARBON; CINEOLE; CYCLOHEXANOL DERIVATIVE; CYTOCHROME P-450 176A; CYTOCHROME P450; OXYGEN; TERPENE;

BATCH CELL CULTURE; BIOREACTOR; BIOSYNTHESIS; BIOTRANSFORMATION; CITROBACTER; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; HYDROXYLATION; METABOLIC ENGINEERING; METABOLISM; PSEUDOMONAS PUTIDA;

BATCH CELL CULTURE TECHNIQUES; BIOREACTORS; BIOTRANSFORMATION; CARBON; CITROBACTER; CYCLOHEXANOLS; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI; HYDROXYLATION; METABOLIC ENGINEERING; MONOTERPENES; OXYGEN; PSEUDOMONAS PUTIDA;

EID: 84975758254     PISSN: 09593993     EISSN: 15730972     Source Type: Journal    
DOI: 10.1007/s11274-016-2071-y     Document Type: Article

References (60)

1. Alonso-Gutierrez J, Chan R, Batth TS, Adams PD, Keasling JD, Petzold CJ, Lee TS (2013) Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab Eng 19:33–41. doi:10.1016/j.ymben.2013.05.004
2. Anfelt J, Hallström B, Nielsen J, Uhlén M, Hudson EP (2013) Using transcriptomics to improve butanol tolerance of Synechocystis sp. Strain PCC 6803. Appl Environ Microbiol 79:7419–7427. doi:10.1128/AEM.02694-13
3. Azerad R (2014) 1,8-Cineole: chemical and biological oxidation reactions and products. Chempluschem 79:634–655. doi:10.1002/cplu.201300422
4. Bagdasarian M, Lurz R, Ruckert B, Franklin FC, Frey J, Timmis KN (1981) Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF 1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. Gene 16:237–247. doi:10.1016/0378-1119(81)90079-2
5. Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475. doi:10.1016/j.fct.2007.09.106
6. Bormann S, Etschmann MMW, Mirata MA, Schrader J (2012) Integrated bioprocess for the stereospecific production of linalool oxides from linalool with Corynespora cassiicola DSM 62475. J Ind Microbiol Biotechnol 39:1761–1769. doi:10.1007/s10295-012-1181-2
7. Chen B, Ling H, Chang MW (2013) Transporter engineering for improved tolerance against alkane biofuels in Saccharomyces cerevisiae. Biotechnol Biofuels 6:21. doi:10.1186/1754-6834-6-21
8. Choi SY (2012) Inhibitory effects of geranic acid derivatives on melanin biosynthesis. J Cosmet Sci 63:351–358
9. Choi KH, 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. doi:10.1016/j.mimet.2005.06.001
10. Cornelissen S, Liu S, Deshmukh AT, Schmid A, Bühler B (2011) Cell physiology rather than enzyme kinetics can determine the efficiency of cytochrome P450-catalyzed C–H-oxyfunctionalization. J Ind Microbiol Biotechnol 38:1359–1370. doi:10.1007/s10295-010-0919-y
11. Cornelissen S, Julsing MK, Volmer J, Riechert O, Schmid A, Bühler B (2013) Whole-cell-based CYP153A6-catalyzed (S)-limonene hydroxylation efficiency depends on host background and profits from monoterpene uptake via AlkL. Biotechnol Bioeng 110:1282–1292. doi:10.1002/bit.24801
12. Davis EM, Croteau R (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Topics Curr Chem 209:53–95
13. Doukyu N, Ishikawa K, Watanabe R, Ogino H (2012) Improvement in organic solvent tolerance by double disruptions of proV and marR genes in Escherichia coli. J Appl Microbiol 112:464–474. doi:10.1111/j.1365-2672.2012.05236.x
14. Dower WJ, Miller JF, Ragsdale CW (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16:6127–6145. doi:10.1002/cbic.200700325
15. Dragosits M, Mattanovich D (2013) Adaptive laboratory evolution—principles and applications for biotechnology. Microb Cell Fact 12:64. doi:10.1186/1475-2859-12-64
16. Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487. doi:10.1038/msb.2011.21
17. Fernández M, Duque E, Pizarro-Tobías P, Van Dillewijn P, Wittich RM, Ramos JL (2009) Microbial responses to xenobiotic compounds. Identification of genes that allow Pseudomonas putida KT2440 to cope with 2,4,6-trinitrotoluene. Microb Biotechnol 2:287–294. doi:10.1111/j.1751-7915.2009.00085.x
18. Fernández M, Conde S, De La Torre J, Molina-Santiago C, Ramos JL, Duque E (2012) Mechanisms of resistance to chloramphenicol in Pseudomonas putida KT2440. Antimicrob Agents Chemother 56:1001–1009. doi:10.1128/AAC.05398-11
19. Foo JL, Jensen HM, Dahl RH, George K, Keasling JD, Lee TS, Leong S, Mukhopadhyay A (2014) Improving microbial biogasoline production in Escherichia coli using tolerance engineering. MBio 5:e01932-14. doi:10.1128/mBio.01932-14
20. Hawkes DB, Adams GW, Burlingame AL, Ortiz De Montellano PR, De Voss JJ (2002) Cytochrome P450cin (CYP176A), isolation, expression, and characterization. J Biol Chem 277:27725–27732. doi:10.1074/jbc.M203382200
21. Hawkes DB, Slessor KE, Bernhardt PV, De Voss JJ (2010) Cloning, expression and purification of cindoxin, an unusual FMN-containing cytochrome P450 redox partner. ChemBioChem 11:1107–1114. doi:10.1002/cbic.201000119
22. Jeske M, Altenbuchner J (2010) The Escherichia coli rhamnose promoter rhaPBAD is in Pseudomonas putida KT2440 independent of Crp-cAMP activation. Appl Microbiol Biotechnol 85:1923–1933. doi:10.1007/s00253-009-2245-8
23. Kang A, Chang MW (2012) Identification and reconstitution of genetic regulatory networks for improved microbial tolerance to isooctane. Mol BioSyst 8:1350. doi:10.1039/c2mb05441h
24. Lin L, Ji Y, Tu Q, Huang R, Teng L, Zeng X, Song H, Wang K, Zhou Q, Li Y, Cui Q, He Z, Zhou J, Xu J (2013) Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter. Biotechnol Biofuels 6:103. doi:10.1186/1754-6834-6-103
25. MacRae IC, Alberts V, Carman RM, Shaw IM (1979) Products of 1,8-cineole oxidation by a pseudomonad. Aust J Chem 32:917–922. doi:10.1071/CH9790917
26. Mahmoud SS, Croteau RB (2002) Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci 7:366–373
27. Mars A, Gorissen JPL, van den Beld I, Eggink G (2001) Bioconversion of limonene to increased concentrations of perillic acid by Pseudomonas putida GS1 in a fed-batch reactor. Appl Microbiol Biotechnol 56:101–107. doi:10.1007/s002530100625
28. Martínez-García E, Nikel P, Aparicio T, de Lorenzo V (2014a) Pseudomonas 2.0: genetic upgrading of P. putida KT2440 as an enhanced host for heterologous gene expression. Microb Cell Fact 13:159. doi:10.1186/s12934-014-0159-3
29. Martínez-García E, Nikel PI, Chavarría M, de Lorenzo V (2014b) The metabolic cost of flagellar motion in Pseudomonas putida KT2440. Environ Microbiol 16:291–303. doi:10.1111/1462-2920.12309
30. 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 13:1–11. doi:10.1186/s12934-014-0170-8
31. Mirata MA, Heerd D, Schrader J (2009) Integrated bioprocess for the oxidation of limonene to perillic acid with Pseudomonas putida DSM 12264. Process Biochem 44:764–771. doi:10.1016/j.procbio.2009.03.013
32. Miyazawa M, Hashimoto Y (2002) Antimicrobial and bactericidal activities of esters of 2-endo-hydroxy-1,8-cineole as new aroma chemicals. J Agric Food Chem 50:3522–3526. doi:10.1021/jf011555w
33. Miyazawa M, Kameoka H, Morinaga K, Negoro K, Mura N (1989) Hydroxycineole: four new metabolites of 1,8-cineole in rabbits. J Agric Food Chem 37:222–226. doi:10.1021/jf00085a051
34. Molina G, Pimentel MR, Pastore GM (2013) Pseudomonas: a promising biocatalyst for the bioconversion of terpenes. Appl Microbiol Biotechnol 97:1851–1864. doi:10.1007/s00253-013-4701-8
35. Nakazawa T (2002) Travels of a Pseudomonas, from Japan around the world. Environ Microbiol 4:782–786. doi:10.1046/j.1462-2920.2002.00310.x
36. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VAP, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen J, Timmis KN, Düsterhöft A, Tümmler B, Fraser CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4:799–808. doi:10.1046/j.1462-2920.2002.00366.x
37. Oh HY, Lee JO, Bin Kim O (2012) Increase of organic solvent tolerance of Escherichia coli by the deletion of two regulator genes, fadR and marR. Appl Microbiol Biotechnol 96:1619–1627. doi:10.1007/s00253-012-4463-8
38. Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence. J Biol Chem 239:2370–2378
39. Patel T, Ishiuji Y, Yosipovitch G (2007) Menthol: a refreshing look at this ancient compound. J Am Acad Dermatol 57:873–878. doi:10.1016/j.jaad.2007.04.008
40. Ramos JL, Duque E, Gallegos M-T, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 56:743–768. doi:10.1146/annurev.micro.56.012302.161038
41. Rodriguez P, Sierra W, Rodriguez S, Menendez P (2006) Biotransformation of 1,8-cineole, the main product of Eucalyptus oils. Electron J Biotechnol 9:232–236. doi:10.2225/vol9-issue3-fulltext-28
42. Saxena D, Joshi N, Srivastava S (2002) Mechanism of copper resistance in a copper mine isolate Pseudomonas putida strain S4. Curr Microbiol 45:410–414. doi:10.1007/s00284-002-3787-5
43. Schewe H, Mirata MA, Holtmann D, Schrader J (2011) Biooxidation of monoterpenes with bacterial monooxygenases. Process Biochem 46:1885–1899. doi:10.1016/j.procbio.2011.06.010
44. Schewe H, Mirata M, Schrader J (2015) Bioprocess engineering for microbial synthesis and conversion of isoprenoids. In: Schrader J, Bohlmann J (eds) Biotechnology of isoprenoids SE-321. Springer, Heidelberg, pp 251–286
45. Schrader J (2007) Microbial flavour production. In: Berger RG (ed) Flavours and fragrances. Springer, Berlin Heidelberg, pp 507–574
46. Slessor KE, Hawkes DB, Farlow A, Pearson AG, Stok JE, De Voss JJ (2012) An in vivo cytochrome P450 cin (CYP176A1) catalytic system for metabolite production. J Mol Catal B Enzym 79:15–20. doi:10.1016/j.molcatb.2012.03.007
47. Someya Y, Kobayashi A, Kubota K (2001) Isolation and identification of trans-2- and trans-3-hydroxy-1,8-cineole glucosides from Alpinia galanga. Biosci Biotechnol Biochem 65:950–953. doi:10.1271/bbb.65.950
48. Southwell IA, Maddox CDA, Zalucki MP (1995) Metabolism of 1,8-cineole in tea tree (Melaleuca alternifolia and M. linariifolia) by pyrgo beetle (Paropsisterna tigrina). J Chem Ecol 21:439–453
49. Southwell I, Russell MF, Maddox CD, Wheeler GS (2003) Differential metabolism of 1,8-cineole in insects. J Chem Ecol 29:83–94
50. Speelmans G, Bijlsma A, Eggink G (1998) Limonene bioconversion to high concentrations of a single and stable product, perillic acid, by a solvent-resistant Pseudomonas putida strain. Appl Microbiol Biotechnol 50:538–544. doi:10.1007/s002530051331
51. Tomas CA, Welker NE, Papoutsakis ET (2003) Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell’s transcriptional program. Appl Environ Microbiol 69:4951–4965. doi:10.1128/AEM.69.8.4951-4965.2003
52. Udaondo Z, Duque E, Fernández M, Molina L, La Torre JD, Bernal P, Niqui JL, Pini C, Roca A, Matilla MA, Antonia Molina-Henares M, Silva-Jiménez H, Navarro-Avilés G, Busch A, Lacal J, Krell T, Segura A, Ramos JL (2012) Analysis of solvent tolerance in Pseudomonas putida DOT-T1E based on its genome sequence and a collection of mutants. FEBS Lett 586(18):2932–2938
53. Van Beilen JB, Holtackers R, Lüscher D, Bauer U, Witholt B, Duetz WA (2005) Biocatalytic production of perillyl alcohol from limonene by using a novel Mycobacterium sp. cytochrome P450 alkane hydroxylase expressed in Pseudomonas putida. Appl Environ Microbiol 71:1737–1744. doi:10.1128/AEM.71.4.1737-1744.2005
54. Volmer J, Neumann C, Bühler B, Schmid A (2014) Engineering of Pseudomonas taiwanensis VLB120 for constitutive solvent tolerance and increased specific styrene epoxidation activity. Appl Environ Microbiol 80:6539–6548. doi:10.1128/AEM.01940-14
55. Watanabe R, Doukyu N (2014) Improvement of organic solvent tolerance by disruption of the lon gene in Escherichia coli. J Biosci Bioeng 118:139–144. doi:10.1016/j.jbiosc.2014.01.011
56. Woodruff LBA, May BL, Warner JR, Gill RT (2013) Towards a metabolic engineering strain “commons”: an Escherichia coli platform strain for ethanol production. Biotechnol Bioeng 110:1520–1526. doi:10.1002/bit.24840
57. Yalkowsky SH, He Y, Jain P (2010) Handbook of aqueous solubility data, Second edn. CRC Press, Boca Raton
58. Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119. doi:10.1016/0378-1119(85)90120-9
59. Zengin Çekiç S, Holtmann D, Güven G, Mangold KM, Schwaneberg U, Schrader J (2010) Mediated electron transfer with P450cin. Electrochem Commun 12:1547–1550. doi:10.1016/j.elecom.2010.08.030
60. Zingaro KA, Papoutsakis ET (2012) Toward a semisynthetic stress response system to engineer microbial solvent tolerance. MBio. doi:10.1128/mBio.00308-12