De novo production of the monoterpenoid geranic acid by metabolically engineered Pseudomonas putida

Microbial Cell Factories

Volumn 13, Issue 1, 2014, Pages

  Mi, Jia ^a   Becher, Daniela ^a   Lubuta, Patrice ^a   Dany, Sarah ^a   Tusch, Kerstin ^a   Schewe, Hendrik ^a   Buchhaupt, Markus ^a   Schrader, Jens ^a  

^a DECHEMA FORSCHUNGSINSTITUT   (Germany)

Author keywords

de novo; DSM12264; Geranic acid; Geraniol; Metabolic engineering; Mevalonate pathway; Microbial cell factory; Monoterpene; Monoterpenoid; Pseudomonas putida

Indexed keywords

BACTERIAL ENZYME; COSMETIC; FRAGRANCE; GERANIC ACID; GERANIOL; GERANIOL SYNTHASE; GLYCEROL; ISOPENTENYL DIPHOSPHATE; MEVALONIC ACID; MONOTERPENOID; TERPENOID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BASIL; BIOSYNTHESIS; CARBON SOURCE; CONTROLLED STUDY; ESCHERICHIA COLI; FED BATCH CULTURE; FLAVOR; GENE EXPRESSION; METABOLIC ENGINEERING; MYXOCOCCUS XANTHUS; NONHUMAN; OXIDATION; PROTEIN EXPRESSION; PSEUDOMONAS PUTIDA; SACCHAROMYCES CEREVISIAE; SPECIES COMPARISON;

EID: 84924029106     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-014-0170-8     Document Type: Article

References (68)

1. Bution ML, Molina G, Abrahao MR, Pastore GM: Genetic and metabolic engineering of microorganisms for the development of new flavor compounds from terpenic substrates. Crit Rev Biotechnol 2014:1-13. doi:10.3109/07388551.2013.855161
2. Breitmaier E: Terpene: Aromen, Düfte, Pharmaka, Pheromone. Weinheim: Wiley-VCH; 2005.
3. Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD: Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 2003, 21:796-802.
4. Shiba Y, Paradise EM, Kirby J, Ro DK, Keasling JD: Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab Eng 2007, 9:160-168.
5. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MC, Withers ST, Shiba Y, Sarpong R, Keasling JD: Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440:940-943.
6. Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D, Leavell MD, Tai A, Main A, Eng D, Polichuk DR, Teoh KH, Reed DW, Treynor T, Lenihan J, Fleck M, Bajad S, Dang G, Dengrove D, Diola D, Dorin G, Ellens KW, Fickes S, Galazzo J, Gaucher SP, Geistlinger T, Henry R, Hepp M, Horning T, Iqbal T, et al: High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 2013, 496:528-532.
7. Scalcinati G, Knuf C, Partow S, Chen Y, Maury J, Schalk M, Daviet L, Nielsen J, Siewers V: Dynamic control of gene expression in Saccharomyces cerevisiae engineered for the production of plant sesquitepene α-santalene in a fed-batch mode. Metab Eng 2012, 14:91-103.
8. Anthony JR, Anthony LC, Nowroozi F, Kwon G, Newman JD, Keasling JD: Optimization of the mevalonate-based isoprenoid biosynthetic pathway in Escherichia coli for production of the anti-malarial drug precursor amorpha-4, 11-diene. Metab Eng 2009, 11:13-19.
9. Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS: Identification and microbial production of a terpene-based advanced biofuel. Nat Commun 2011, 2:483.
10. Sarria S, Wong B, Martin HG, Keasling JD, Peralta-Yahya P: Microbial synthesis of pinene. ACS Synth Biol 2014 in press (DOI:10.1021/sb4001382).
11. Yang J, Nie Q, Ren M, Feng H, Jiang X, Zheng Y, Liu M, Zhang H, Xian M: Metabolic engineering of Escherichia coli for the biosynthesis of alpha-pinene. Biotechnol Biofuels 2013, 6:60.
12. van der Werf MJ, De Bont JAM, Leak DJ: Opportunities in microbial biotransformation of monoterpenes. In Biotechnology of Aroma Compounds, Volume 55. Edited by Scheper T. Berlin: Springer; 1997:283.
13. Tippmann S, Chen Y, Siewers V, Nielsen J: From flavors and pharmaceuticals to advanced biofuels: production of isoprenoids in Saccharomyces cerevisiae. Biotechnol J 2013, 8:1435-1444.
14. Trombetta D, Castelli F, Sarpietro MG, Venuti V, Cristani M, Daniele C, Saija A, Mazzanti G, Bisignano G: Mechanisms of antibacterial action of three monoterpenes. Antimicrob Agents Chemother 2005, 49:2474-2478.
15. Uribe S, Ramirez J, Peña A: Effects of beta-pinene on yeast membrane functions. J Bacteriol 1985, 161:1195-1200.
16. Andrews RE, Parks LW, Spence KD: Some effects of Douglas fir terpenes on certain microorganisms. Appl Environ Microbiol 1980, 40:301-304.
17. Brennan TC, Kromer JO, Nielsen LK: Physiological and transcriptional responses of Saccharomyces cerevisiae to d-limonene show changes to the cell wall but not to the plasma membrane. Appl Environ Microbiol 2013, 79:3590-3600.
18. Ramos JL, Duque E, Gallegos M-T, Godoy P, Ramos-González MI, Rojas A, Terán W, Segura A: Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 2002, 56:743-768.
19. Heipieper HJ, Neumann G, Cornelissen S, Meinhardt F: Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 2007, 74:961-973.
20. Poblete-Castro I, Becker J, Dohnt K, Dos Santos VM, Wittmann C: Industrial biotechnology of Pseudomonas putida and related species. Appl Microbiol Biotechnol 2012, 93:2279-2290.
21. Wierckx NJ, Ballerstedt H, de Bont JA, Wery J: Engineering of solvent-tolerant Pseudomonas putida S12 for bioproduction of phenol from glucose. Appl Environ Microbiol 2005, 71:8221-8227.
22. Meijnen JP, Verhoef S, Briedjlal AA, de Winde JH, Ruijssenaars HJ: Improved p-hydroxybenzoate production by engineered Pseudomonas putida S12 by using a mixed-substrate feeding strategy. Appl Microbiol Biotechnol 2011, 90:885-893.
23. Faizal I, Dozen K, Hong CS, Kuroda A, Takiguchi N, Ohtake H, Takeda K, Tsunekawa H, Kato J: Isolation and characterization of solvent-tolerant Pseudomonas putida strain T-57, and its application to biotransformation of toluene to cresol in a two-phase (organic-aqueous) system. J Ind Microbiol Biotechnol 2005, 32:542-547.
24. Mirata MA, Heerd D, Schrader J: Integrated bioprocess for the oxidation of limonene to perillic acid with Pseudomonas putida DSM 12264. Process Biochem 2009, 44:764-771.
25. Speelmans G, Bijlsma A, Eggink G: Limonene bioconversion to high concentrations of a single and stable product, perillic acid, by a solvent-resistant Pseudomonas putida strain. Appl Microbiol Biotechnol 1998, 50:538-544.
26. Bedoukian PZ: Perfumery and Flavoring Synthetics. Wheaton: Allured Publishing Corporation; 1986.
27. Schrader J: Microbial Flavour Production. In Flavours and Fragrances. Edited by Berger RG. Berlin: Springer; 2007:507-574.
28. Yang T, Stoopen G, Yalpani N, Vervoort J, de Vos R, Voster A, Verstappen FW, Bouwmeester HJ, Jongsma MA: Metabolic engineering of geranic acid in maize to achieve fungal resistance is compromised by novel glycosylation patterns. Metab Eng 2011, 13:414-425.
29. Wang N, Hebert DN: Tyrosinase maturation through the mammalian secretory pathway: bringing color to life. Pigment Cell Res 2006, 19:3-18.
30. Choi SY: Inhibitory effects of geranic acid derivatives on melanin biosynthesis. J Cosmet Sci 2012, 63:351-358.
31. Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E: Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol 2004, 134:370-379.
32. Brennan TCR, Turner CD, Krömer JO, Nielsen LK: Alleviating monoterpene toxicity using a two-phase extractive fermentation for the bioproduction of jet fuel mixtures in Saccharomyces cerevisiae. Biotechnol Bioeng 2012, 109:2513-2522.
33. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Santos VAP M d, 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, Lee PC, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, et al: Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 2002, 4:799-808.
34. Schrader J, Berger RG: Biotechnological production of terpenoid flavor and fragrance compounds. In Biotechnology: Special Processes, Volume 10. Edited by Rehm HJ, Reed G. Weinheim: Wiley-VCH; 2001:373-422.
35. Chandran SS, Kealey JT, Reeves CD: Microbial production of isoprenoids. Process Biochem 2011, 46:1703-1710.
36. Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A: Engineering microbial biofuel tolerance and export using efflux pumps. Mol Sys Biol 2011, 7:487.
37. Cantwell SG, Lau EP, Watt DS, Fall RR: Biodegradation of acyclic isoprenoids by Pseudomonas species. J Bacteriol 1978, 135:324-333.
38. Vandenbergh PA, Wright AM: Plasmid involvement in acyclic isoprenoid metabolism by Pseudomonas putida. Appl Environ Microbiol 1983, 45:1953-1955.
39. Forster-Fromme K, Jendrossek D: Identification and characterization of the acyclic terpene utilization gene cluster of Pseudomonas citronellolis. FEMS Microbiol Lett 2006, 264:220-225.
40. Chattopadhyay A, Förster-Fromme K, Jendrossek D: PQQ-Dependent Alcohol Dehydrogenase (QEDH) of Pseudomonas aeruginosa is involved in catabolism of acyclic terpenes. J Basic Microbiol 2010, 50:119-124.
41. Oswald M, Fischer M, Dirninger N, Karst F: Monoterpenoid biosynthesis in Saccharomyces cerevisiae. FEMS Yeast Res 2007, 7:413-421.
42. Fischer MJ, Meyer S, Claudel P, Perrin M, Ginglinger JF, Gertz C, Masson JE, Werck-Reinhardt D, Hugueney P, Karst F: Specificity of Ocimum basilicum geraniol synthase modified by its expression in different heterologous systems. J Biotech 2013, 163:24-29.
43. Fischer MJ, Meyer S, Claudel P, Bergdoll M, Karst F: Metabolic engineering of monoterpene synthesis in yeast. Biotechnol Bioeng 2011, 108:1883-1892.
44. Fischer MJ, Meyer S, Claudel P, Steyer D, Bergdoll M, Hugueney P: Determination of amino-acidic positions important for Ocimum basilicum geraniol synthase activity. Adv Biosci Biotechnol 2013, 4:242-249.
45. Liu J, Zhang W, Du G, Chen J, Zhou J: Overproduction of geraniol by enhanced precursor supply in Saccharomyces cerevisiae. J Biotech 2013, 168:446-451.
46. da Silva GP, Mack M, Contiero J: Glycerol: a promising and abundant carbon source for industrial microbiology. Biotechnol Adv 2009, 27:30-39.
47. Peralta-Yahya PP, Zhang F, Del Cardayre SB, Keasling JD: Microbial engineering for the production of advanced biofuels. Nature 2012, 488:320-328.
48. Morrone D, Lowry L, Determan MK, Hershey DM, Xu M, Peters RJ: Increasing diterpene yield with a modular metabolic engineering system in E. coli: comparison of MEV and MEP isoprenoid precursor pathway engineering. Appl Microbiol Biotechnol 2010, 85:1893-1906.
49. Pitera DJ, Paddon CJ, Newman JD, Keasling JD: Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli. Metab Eng 2007, 9:193-207.
50. Redding-Johanson AM, Batth TS, Chan R, Krupa R, Szmidt HL, Adams PD, Keasling JD, Soon Lee T, Mukhopadhyay A, Petzold CJ: Targeted proteomics for metabolic pathway optimization: application to terpene production. Metab Eng 2011, 13:194-203.
51. Alonso-Gutierrez J, Chan R, Batth TS, Adams PD, Keasling JD, Petzold CJ, Lee TS: Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab Eng 2013, 19:33-41.
52. Tsuruta H, Paddon CJ, Eng D, Lenihan JR, Horning T, Anthony LC, Regentin R, Keasling JD, Renninger NS, Newman JD: High-level production of amorpha-4, 11-diene, a precursor of the antimalarial agent artemisinin, in Escherichia coli. PLoS One 2009, 4:e4489.
53. Zahiri HS, Yoon SH, Keasling JD, Lee SH, Won Kim S, Yoon SC, Shin YC: Coenzyme Q10 production in recombinant Escherichia coli strains engineered with a heterologous decaprenyl diphosphate synthase gene and foreign mevalonate pathway. Metab Eng 2006, 8:406-416.
54. Blanchard L, Karst F: Characterization of a lysine-to-glutamic acid mutation in a conservative sequence of farnesyl diphosphate synthase from Saccharomyces cerevisiae. Gene 1993, 125:185-189.
55. Schmidt A, Gershenzon J: Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 2008, 69:49-57.
56. Nowroozi F, Baidoo EK, Ermakov S, Redding-Johanson A, Batth T, Petzold C, Keasling J: Metabolic pathway optimization using ribosome binding site variants and combinatorial gene assembly. Appl Microbiol Biotechnol 2013, 98:1567-1581.
57. Beuttler H, Hoffmann J, Jeske M, Hauer B, Schmid RD, Altenbuchner J, Urlacher VB: Biosynthesis of zeaxanthin in recombinant Pseudomonas putida. Appl Microbiol Biotechnol 2011, 89:1137-1147.
58. Willrodt C, David C, Cornelissen S, Buhler B, Julsing MK, Schmid A: Engineering the productivity of recombinant Escherichia coli for limonene formation from glycerol in minimal media. Biotechnol J 2014 in press (doi:10.1002/biot.201400023).
59. Myers JA, Curtis BS, Curtis WR: Improving accuracy of cell and chromophore concentration measurements using optical density. BMC Biophys 2013, 6:4.
60. Cornelissen S, Julsing MK, Volmer J, Riechert O, Schmid A, Bühler B: Whole-cell-based CYP153A6-catalyzed (S)-limonene hydroxylation efficiency depends on host background and profits from monoterpene uptake via AlkL. Biotechnol Bioeng 2013, 110:1282-1292.
61. Kim GJ, Lee IY, Choi DK, Yoon SC, Park YH: High cell density cultivation of Pseudomonas putida MB01 using glucose. J Microbiol Biotechnol 1996, 6:221-224.
62. Thuesen MH, Norgaard A, Hansen AM, Caspersen MB, Christensen HE: Expression of recombinant Pseudomonas stutzeri di-heme cytochrome c4 by high-cell-density fed-batch cultivation of Pseudomonas putida. Protein Expr Purif 2003, 27:175-181.
63. Sun Z, Ramsay J, Guay M, Ramsay B: Automated feeding strategies for high-cell-density fed-batch cultivation of Pseudomonas putida KT2440. Appl Microbiol Biotechnol 2006, 71:423-431.
64. Ramadhan S, Matsui T, Nakano K, Minami H: High cell density cultivation of Pseudomonas putida strain HKT554 and its application for optically active sulfoxide production. Appl Microbiol Biotechnol 2013, 97:1903-1907.
65. Entian K-D, Kötter P: 23 yeast mutant and plasmid collections. Methods Microbiol 1998, 26:431-449.
66. Bethesda_Research_Laboratories: BRL pUC host: E. coli DH5α™ competent cells. Bethesda Res Lab Focus 1986, 8:9-12.
67. Jeske M, Altenbuchner J: The Escherichia coli rhamnose promoter rhaP(BAD) is in Pseudomonas putida KT2440 independent of Crp-cAMP activation. Appl Microbiol Biotechnol 2010, 85:1923-1933.
68. Choi KH, Kumar A, Schweizer HP: 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 2006, 64:391-397.