Enabling technologies to advance microbial isoprenoid production

Advances in Biochemical Engineering/Biotechnology

Volumn 148, Issue , 2015, Pages 143-160

  Chen, Yun ^a   Zhou, Yongjin J ^a   Siewers, Verena ^a   Nielsen, Jens ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

E. coli; Enabling technologies; Metabolic engineering; S. cerevisiae; Sesquiterpenes; Terpenoids

Indexed keywords

TERPENE;

ALGORITHM; BACTERIUM; BIOMASS; CHEMISTRY; ESCHERICHIA COLI; FERMENTATION; METABOLIC ENGINEERING; METABOLISM; MICROBIOLOGY; PROCEDURES; SACCHAROMYCES CEREVISIAE; SYNTHETIC BIOLOGY; SYSTEMS BIOLOGY;

ALGORITHMS; BACTERIA; BIOMASS; ESCHERICHIA COLI; FERMENTATION; INDUSTRIAL MICROBIOLOGY; METABOLIC ENGINEERING; SACCHAROMYCES CEREVISIAE; SYNTHETIC BIOLOGY; SYSTEMS BIOLOGY; TERPENES;

EID: 84930201218     PISSN: 07246145     EISSN: None     Source Type: Book Series    
DOI: 10.1007/10_2014_284     Document Type: Article

References (83)

1. Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54(4):656–669
2. Chang MC, Keasling JD (2006) Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol 2(12):674–681
3. Tippmann S, Chen Y, Siewers V, Nielsen J (2013) From flavors and pharmaceuticals to advanced biofuels: production of isoprenoids in Saccharomyces cerevisiae. Biotechnol J 8 (12):1435–1444
4. Maury J, Asadollahi MA, Møller K, Clark A, Nielsen J (2005) Microbial isoprenoid production: an example of green chemistry through metabolic engineering. Adv Biochem Eng Biotechnol 100:19–51
5. 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, Jiang H, Kizer L, Lieu B, Melis D, Moss N, Regentin R, Secrest S, Tsuruta H, Vazquez R, Westblade LF, Xu L, Yu M, Zhang Y, Zhao L, Lievense J, Covello PS, Keasling JD, Reiling KK, Renninger NS, Newman JD (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496 (7446):528–532
6. Guerra-Bubb J, Croteau R, Williams RM (2012) The early stages of taxol biosynthesis: an interim report on the synthesis and identification of early pathway metabolites. Nat Prod Rep 29(6):683–696
7. Gao W, Hillwig ML, Huang L, Cui G, Wang X, Kong J, Yang B, Peters RJ (2009) A functional genomics approach to tanshinone biosynthesis provides stereochemical insights. Org Lett 11(22):5170–5173
8. Jennewein S, Rithner CD, Williams RM, Croteau RB (2001) Taxol biosynthesis: Taxane 13 alpha-hydroxylase is a cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci USA 98(24):13595–13600
9. Zerbe P, Hamberger B, Yuen MM, Chiang A, Sandhu HK, Madilao LL, Nguyen A, Hamberger B, Bach SS, Bohlmann J (2013) Gene discovery of modular diterpene metabolism in nonmodel systems. Plant Physiol 162(2):1073–1091
10. Chen S, Xu J, Liu C, Zhu Y, Nelson DR, Zhou S, Li C, Wang L, Guo X, Sun Y, Luo H, Li Y, Song J, Henrissat B, Levasseur A, Qian J, Li J, Luo X, Shi L, He L, Xiang L, Xu X, Niu Y, Li Q, Han MV, Yan H, Zhang J, Chen H, Lv A, Wang Z, Liu M, Schwartz DC, Sun C (2012) Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 3:913
11. Guo J, Zhou YJ, Hillwig ML, Shen Y, Yang L, Wang Y, Zhang X, Liu W, Peters RJ, Chen X, Zhao ZK, Huang L (2013) CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts. Proc Natl Acad Sci USA 110(29):12108–12113
12. 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 (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440 (7086):940–943
13. Brustad EM, Arnold FH (2011) Optimizing non-natural protein function with directed evolution. Curr Opin Chem Biol 15(2):201–210
14. Savile CK, Janey JM, Mundorff EC, Moore JC, Tam S, Jarvis WR, Colbeck JC, Krebber A, Fleitz FJ, Brands J, Devine PN, Huisman GW, Hughes GJ (2010) Biocatalytic asymmetric synthesis of chiral amines from ketones applied to sitagliptin manufacture. Science 329 (5989):305–309
15. Coelho PS, Brustad EM, Kannan A, Arnold FH (2013) Olefin cyclopropanation via carbene transfer catalyzed by engineered cytochrome P450 enzymes. Science 339(6117):307–310
16. Coelho PS, Wang ZJ, Ener ME, Baril SA, Kannan A, Arnold FH, Brustad EM (2013) A serine-substituted P450 catalyzes highly efficient carbene transfer to olefins in vivo. Nat Chem Biol 9(8):485–487
17. Lauchli R, Rabe KS, Kalbarczyk KZ, Tata A, Heel T, Kitto RZ, Arnold FH (2013) Highthroughput screening for terpene-synthase-cyclization activity and directed evolution of a terpene synthase. Angew Chem Int Ed 52(21):5571–5574
18. Hult K, Berglund P (2007) Enzyme promiscuity: mechanism and applications. Trends Biotechnol 25(5):231–238
19. Dietrich JA, Yoshikuni Y, Fisher KJ, Woolard FX, Ockey D, McPhee DJ, Renninger NS, Chang MCY, Baker D, Keasling JD (2009) A novel semi-biosynthetic route for artemisinin production using engineered substrate-promiscuous P450(BM3). ACS Chem Biol 4(4):261–267
20. Yao YF, Wang CS, Qiao J, Zhao GR (2013) Metabolic engineering of Escherichia coli for production of salvianic acid A via an artificial biosynthetic pathway. Metab Eng 19:79–87
21. Tsuruta H, Paddon CJ, Eng D, Lenihan JR, Horning T, Anthony LC, Regentin R, Keasling JD, Renninger NS, Newman JD (2009) High-level production of amorpha-4,11-diene, a precursor of the antimalarial agent artemisinin, in Escherichia coli. PLoS ONE 4(2):e4489
22. Whited GM, Feher FJ, Benko DA, Cervin MA, Chotani GK, McAuliffe JC, LaDuca RJ, Ben- Shoshan EA, Sanford KJ (2010) Technology update: development of a gas-phase bioprocess for isoprene-monomer production using metabolic pathway engineering. Ind Biotechnol 6 (3):152–163
23. Chang MC, Eachus RA, Trieu W, Ro DK, Keasling JD (2007) Engineering Escherichia coli for production of functionalized terpenoids using plant P450s. Nat Chem Biol 3(5):274–277
24. Heider SA, Peters-Wendisch P, Wendisch VF (2012) Carotenoid biosynthesis and overproduction in Corynebacterium glutamicum. BMC Microbiol 12:198
25. Zhou K, Zou R, Zhang C, Stephanopoulos G, Too HP (2013) Optimization of amorphadiene synthesis in bacillus subtilis via transcriptional, translational, and media modulation. Biotechnol Bioeng 110(9):2556–2561
26. Dai Z, Liu Y, Zhang X, Shi M, Wang B, Wang D, Huang L, Zhang X (2013) Metabolic engineering of Saccharomyces cerevisiae for production of ginsenosides. Metab Eng 20:146–156
27. Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou YJ, Jin G, Ye M, Zou H, Zhao ZK (2012) A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun 3:1112
28. Shao Z, Zhao H, Zhao H (2009) DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways. Nucleic Acids Res 37(2):e16
29. Sd Kok, Stanton LH, Slaby T, Durot M, Holmes VF, Patel KG, Platt D, Shapland EB, Serber Z, Dean J, Newman JD, Chandran SS (2014) Rapid and reliable DNA assembly via ligase cycling reaction. ACS Synthetic Biology 3(2):97–106
30. Akada R, Kitagawa T, Kaneko S, Toyonaga D, Ito S, Kakihara Y, Hoshida H, Morimura S, Kondo A, Kida K (2006) PCR-mediated seamless gene deletion and marker recycling in Saccharomyces cerevisiae. Yeast 23(5):399–405
31. Kuijpers NG, Chroumpi S, Vos T, Solis-Escalante D, Bosman L, Pronk JT, Daran JM, Daran- Lapujade P (2013) One-step assembly and targeted integration of multigene constructs assisted by the I-SceI meganuclease in Saccharomyces cerevisiae. FEMS Yeast Res 13(8):769–781
32. Xu P, Vansiri A, Bhan N, Koffas MAG (2012) EPathBrick: a synthetic biology platform for engineering metabolic pathways in E. coli. ACS Synth Biol 1(7):256–266
33. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97(12):6640–6645
34. Lin X, Wang Y, Zhang S, Zhu Z, Zhou YJ, Yang F, Sun W, Wang X, Zhao ZK (2014) Functional integration of multiple genes into the genome of the oleaginous yeast Rhodosporidium toruloides. FEMS Yeast Res doi:10.1111/1567-1364.12140
35. Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD (2003) Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 21(7):796–802
36. Pitera DJ, Paddon CJ, Newman JD, Keasling JD (2007) Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli. Metab Eng 9(2):193–207
37. Maury J, Asadollahi MA, Møller K, Schalk M, Clark A, Formenti LR, Nielsen J (2008) Reconstruction of a bacterial isoprenoid biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett 582(29):4032–4038
38. Partow S, Siewers V, Daviet L, Schalk M, Nielsen J (2012) Reconstruction and evaluation of the synthetic bacterial MEP pathway in Saccharomyces cerevisiae. PLoS ONE 7(12):e52498
39. Asadollahi MA, Maury J, Moller K, Nielsen KF, Schalk M, Clark A, Nielsen J (2008) Production of plant sesquiterpenes in Saccharomyces cerevisiae: effect of ERG9 repression on sesquiterpene biosynthesis. Biotechnol Bioeng 99(3):666–677
40. Asadollahi MA, Maury J, Schalk M, Clark A, Nielsen J (2010) Enhancement of farnesyl diphosphate pool as direct precursor of sesquiterpenes through metabolic engineering of the mevalonate pathway in Saccharomyces cerevisiae. Biotechnol Bioeng 106(1):86–96
41. Paradise EM, Kirby J, Chan R, Keasling JD (2008) Redirection of flux through the FPP branch-point in Saccharomyces cerevisiae by down-regulating squalene synthase. Biotechnol Bioeng 100(2):371–378
42. Keasling J, Newman J, Pitera D (2010) Method for enhancing production of isoprenoid compounds. US 7670825 B2
43. Westfall PJ, Pitera DJ, Lenihan JR, Eng D, Woolard FX, Regentin R, Horning T, Tsuruta H, Melis DJ, Owens A, Fickes S, Diola D, Benjamin KR, Keasling JD, Leavell MD, McPhee DJ, Renninger NS, Newman JD, Paddon CJ (2012) Production of amorphadiene in yeast, and its conversion to dihydroartemisinic acid, precursor to the antimalarial agent artemisinin. Proc Natl Acad Sci USA 109(3):E111–E118
44. Renninger NS, McPhee DJ (2008) Fuel compositions comprising farnesane and farnesane derivatives and method of making and using same. United States Patent
45. Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS (2011) Identification and microbial production of a terpene-based advanced biofuel. Nat Commun 2:483
46. Chen Y, Daviet L, Schalk M, Siewers V, Nielsen J (2013) Establishing a platform cell factory through engineering of yeast acetyl-CoA metabolism. Metab Eng 15:48–54
47. Chen Y, Siewers V, Nielsen J (2012) Profiling of cytosolic and peroxisomal acetyl-CoA metabolism in Saccharomyces cerevisiae. PLoS ONE 7(8):e42475
48. Shiba Y, Paradise EM, Kirby J, Ro DK, Keasing JD (2007) Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab Eng 9(2):160–168
49. Krivoruchko A, Serrano-Amatriain C, Chen Y, Siewers V, Nielsen J (2013) Improving biobutanol production in engineered Saccharomyces cerevisiae by manipulation of acetyl- CoA metabolism. J Ind Microbiol Biotechnol 40(9):1051–1056
50. Kocharin K, Chen Y, Siewers V, Nielsen J (2012) Engineering of acetyl-CoA metabolism for the improved production of polyhydroxybutyrate in Saccharomyces cerevisiae. AMB Express 2(1):52
51. Kozak BU, van Rossum HM, Benjamin KR, Wu L, Daran J-MG, Pronk JT, van Maris AJA (2014) Replacement of the Saccharomyces cerevisiae acetyl-CoA synthetases by alternative pathways for cytosolic acetyl-CoA synthesis. Metab Eng 21:46–59
52. Ajikumar PK, Xiao WH, Tyo KE, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G (2010) Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli. Science 330(6000):70–74
53. Zhou YJ, Gao W, Rong Q, Jin G, Chu H, Liu W, Yang W, Zhu Z, Li G, Zhu G, Huang L, Zhao ZK (2012) Modular pathway engineering of diterpenoid synthases and the mevalonic acid pathway for miltiradiene production. J Am Chem Soc 134(6):3234–3241
54. Xu P, Gu Q, Wang W, Wong L, Bower AG, Collins CH, Koffas MA (2013) Modular optimization of multi-gene pathways for fatty acids production in E. coli. Nat Commun 4:1409
55. Wu J, Du G, Zhou J, Chen J (2013) Metabolic engineering of Escherichia coli for (2S)- pinocembrin production from glucose by a modular metabolic strategy. Metab Eng 16(1):48–55
56. Albertsen L, Chen Y, Bach LS, Rattleff S, Maury J, Brix S, Nielsen J, Mortensen UH (2011) Diversion of flux toward sesquiterpene production in Saccharomyces cerevisiae by fusion of host and heterologous enzymes. Appl Environ Microbiol 77(3):1033–1040
57. Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KL, Keasling JD (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27(8):753–759
58. Delebecque CJ, Lindner AB, Silver PA, Aldaye FA (2011) Organization of intracellular reactions with rationally designed RNA assemblies. Science 333(6041):470–474
59. Conrado RJ, Wu GC, Boock JT, Xu H, Chen SY, Lebar T, Turnek J, Tomšič N, Avbelj M, Gaber R, Koprivnjak T, Mori J, Glavnik V, Vovk I, Beninča M, Hodnik V, Anderluh G, Dueber JE, Jerala R, Delisa MP (2012) DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency. Nucleic Acids Res 40(4):1879–1889
60. Farhi M, Marhevka E, Masci T, Marcos E, Eyal Y, Ovadis M, Abeliovich H, Vainstein A (2011) Harnessing yeast subcellular compartments for the production of plant terpenoids. Metab Eng 13(5):474–481
61. Avalos JL, Fink GR, Stephanopoulos G (2013) Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat Biotech 31 (4):335–341
62. Ma SM, Garcia DE, Redding-Johanson AM, Friedland GD, Chan R, Batth TS, Haliburton JR, Chivian D, Keasling JD, Petzold CJ, Lee TS, Chhabra SR (2011) Optimization of a heterologous mevalonate pathway through the use of variant HMG-CoA reductases. Metab Eng 13(5):588–597
63. Asadollahi MA, Maury J, Patil KR, Schalk M, Clark A, Nielsen J (2009) Enhancing sesquiterpene production in Saccharomyces cerevisiae through in silico driven metabolic engineering. Metab Eng 11(6):328–334
64. Scalcinati G, Partow S, Siewers V, Schalk M, Daviet L, Nielsen J (2012) Combined metabolic engineering of precursor and co-factor supply to increase alpha-santalene production by Saccharomyces cerevisiae. Microb Cell Fact 11:117
65. Ehsani M, Fernández MR, Biosca JA, Dequin S (2009) Reversal of coenzyme specificity of 2,3-butanediol dehydrogenase from Saccharomyces cerevisae and in vivo functional analysis. Biotechnol Bioeng 104(2):381–389
66. Alper H, Jin Y-S, Moxley JF, Stephanopoulos G (2005) Identifying gene targets for the metabolic engineering of lycopene biosynthesis in Escherichia coli. Metab Eng 7(3):155–164
67. Patil KR, Rocha I, Forster J, Nielsen J (2005) Evolutionary programming as a platform for in silico metabolic engineering. BMC Bioinform 6:308
68. Choi HS, Lee SY, Kim TY, Woo HM (2010) In silico identification of gene amplification targets for improvement of lycopene production. Appl Environ Microbiol 76(10):3097–3105
69. Lewis NE, Nagarajan H, Palsson BO (2012) Constraining the metabolic genotype-phenotype relationship using a phylogeny of in silico methods. Nat Rev Microbiol 10(4):291–305
70. Nielsen J, Jewett MC (2008) Impact of systems biology on metabolic engineering of Saccharomyces cerevisiae. FEMS Yeast Res 8(1):122–131
71. Tyo KE, Kocharin K, Nielsen J (2010) Toward design-based engineering of industrial microbes. Curr Opin Microbiol 13(3):255–262
72. Bordel S, Agren R, Nielsen J (2010) Sampling the solution space in genome-scale metabolic networks reveals transcriptional regulation in key enzymes. PLoS Comput Biol 6(7):e1000859
73. Patil KR, Nielsen J (2005) Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc Natl Acad Sci USA 102(8):2685–2689
74. Dahl RH, Zhang F, Alonso-Gutierrez J, Baidoo E, Batth TS, Redding-Johanson AM, Petzold CJ, Mukhopadhyay A, Lee TS, Adams PD, Keasling JD (2013) Engineering dynamic pathway regulation using stress-response promoters. Nat Biotechnol 31(11):1039–1046
75. Redding-Johanson AM, Batth TS, Chan R, Krupa R, Szmidt HL, Adams PD, Keasling JD, Soon Lee T, Mukhopadhyay A, Petzold CJ (2011) Targeted proteomics for metabolic pathway optimization: application to terpene production. Metab Eng 13(2):194–203
76. Fuhrer T, Heer D, Begemann B, Zamboni N (2011) High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal Chem 83(18):7074–7080
77. Canelas AB, Harrison N, Fazio A, Zhang J, Pitkanen JP, van den Brink J, Bakker BM, Bogner L, Bouwman J, Castrillo JI, Cankorur A, Chumnanpuen P, Daran-Lapujade P, Dikicioglu D, van Eunen K, Ewald JC, Heijnen JJ, Kirdar B, Mattila I, Mensonides FI, Niebel A, Penttila M, Pronk JT, Reuss M, Salusjarvi L, Sauer U, Sherman D, Siemann-Herzberg M, Westerhoff H, de Winde J, Petranovic D, Oliver SG, Workman CT, Zamboni N, Nielsen J (2010) Integrated multilaboratory systems biology reveals differences in protein metabolism between two reference yeast strains. Nat Commun 1(9):145
78. Kizer L, Pitera DJ, Pfleger BF, Keasling JD (2008) Application of functional genomics to pathway optimization for increased isoprenoid production. Appl Environ Microbiol 74 (10):3229–3241
79. Brennan TCR, Turner CD, Kromer JO, Nielsen LK (2012) Alleviating monoterpene toxicity using a two-phase extractive fermentation for the bioproduction of jet fuel mixtures in Saccharomyces cerevisiae. Biotechnol Bioeng 109(10):2513–2522
80. 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
81. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314 (5805):1565–1568
82. Newman JD, Marshall J, Chang M, Nowroozi F, Paradise E, Pitera D, Newman KL, Keasling JD (2006) High-level production of amorpha-4,11-diene in a two-phase partitioning bioreactor of metabolically engineered Escherichia coli. Biotechnol Bioeng 95(4):684–691
83. Stark D, von Stockar U (2003) In situ product removal (ISPR) in whole cell biotechnology during the last twenty years. Adv Biochem Eng Biotechnol 80:149–175