Photosynthetic conversion of CO2 to farnesyl diphosphate-derived phytochemicals (amorpha-4,11-diene and squalene) by engineered cyanobacteria

Biotechnology for Biofuels

Volumn 9, Issue 1, 2016, Pages

  Choi, Sun Young ^a   Lee, Hyun Jeong ^a   Choi, Jaeyeon ^a   Kim, Jiye ^a,b   Sim, Sang Jun ^b   Um, Youngsoon ^a   Kim, Yunje ^a   Lee, Taek Soon ^c,d   Keasling, Jay D ^c,d,e,f   Woo, Han Min ^g  

^a Korea Institute of Science and Technology   (South Korea)

^b Korea University   (South Korea)

^c JOINT BIOENERGY INSTITUTE   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e University of California   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g Sungkyunkwan University   (South Korea)

Author keywords

Cyanobacteria; Isoprenoids; Metabolic engineering; Synthetic biology

Indexed keywords

CARBON DIOXIDE; CELL ENGINEERING; GENE EXPRESSION; LIPIDS; METABOLISM; SELENIUM COMPOUNDS; SOLAR CELLS;

CYANOBACTERIA; FARNESYL DIPHOSPHATE SYNTHASE; ISOPRENOIDS; METHYLERYTHRITOL PHOSPHATE PATHWAYS; PHOTOSYNTHETIC PRODUCTION; SYNECHOCOCCUS ELONGATUS; SYNTHETIC BIOLOGY; VALUE-ADDED CHEMICALS;

METABOLIC ENGINEERING;

BIOENGINEERING; CARBON DIOXIDE; CYANOBACTERIUM; GENE EXPRESSION; ISOPRENOID; METABOLISM; PHOTOSYNTHESIS; PHYTOCHEMISTRY;

AMORPHA; CYANOBACTERIA; SYNECHOCOCCUS ELONGATUS PCC 7942;

EID: 85009121364     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-016-0617-8     Document Type: Article

References (65)

1. Kirby J, Keasling JD. Biosynthesis of plant isoprenoids: perspectives for microbial engineering. Annu Rev Plant Biol. 2009;60:335–55.
2. Aharoni A, Jongsma MA, Bouwmeester HJ. Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci. 2005;10(12):594–602.
3. Lavy M, Zuker A, Lewinsohn E, Larkov O, Ravid U, Vainstein A, et al. Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene. Mol Breed. 2002;9(2):103–11.
4. Davidovich-Rikanati R, Lewinsohn E, Bar E, Iijima Y, Pichersky E, Sitrit Y. Overexpression of the lemon basil alpha-zingiberene synthase gene increases both mono- and sesquiterpene contents in tomato fruit. Plant J. 2008;56(2):228–38.
5. Ohara K, Ujihara T, Endo T, Sato F, Yazaki K. Limonene production in tobacco with Perilla limonene synthase cDNA. J Exp Bot. 2003;54(393):2635–42.
6. Ram M, Khan MA, Jha P, Khan S, Kiran U, Ahmad MM, et al. HMG-CoA reductase limits artemisinin biosynthesis and accumulation in Artemisia annua L. plants. Acta Physiol Plant. 2010;32(5):859–66.
7. Ma CF, Wang HH, Lu X, Wang H, Xu GW, Liu BY. Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry. Metabolomics. 2009;5(4):497–506.
8. Zhang L, Jing FY, Li FP, Li MY, Wang YL, Wang GF, et al. Development of transgenic Artemisia annua (Chinese wormwood) plants with an enhanced content of artemisinin, an effective anti-malarial drug, by hairpin-RNA-mediated gene silencing. Biotechnol Appl Biochem. 2009;52:199–207.
9. Farhi M, Marhevka E, Ben-Ari J, Algamas-Dimantov A, Liang Z, Zeevi V, et al. Generation of the potent anti-malarial drug artemisinin in tobacco. Nat Biotechnol. 2011;29(12):1072–4.
10. Salmon M, Laurendon C, Vardakou M, Cheema J, Defernez M, Green S, et al. Emergence of terpene cyclization in Artemisia annua. Nat Commun. 2015;6:6143.
11. Kim SW, Keasling JD. Metabolic engineering of the nonmevalonate isopentenyl diphosphate synthesis pathway in Escherichia coli enhances lycopene production. Biotechnol Bioeng. 2001;72(4):408–15.
12. Alper H, Miyaoku K, Stephanopoulos G. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat Biotechnol. 2005;23(5):612–6.
13. Choi HS, Lee SY, Kim TY, Woo HM. In silico identification of gene amplification targets for improvement of lycopene production. Appl Environ Microb. 2010;76(10):3097–105.
14. Alonso-Gutierrez J, Chan R, Batth TS, Adams PD, Keasling JD, Petzold CJ, et al. Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab Eng. 2013;19:33–41.
15. Sarria S, Wong B, Martin HG, Keasling JD, Peralta-Yahya P. Microbial synthesis of pinene. Acs Synth Biol. 2014;3(7):466–75.
16. 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(7):796–802.
17. Wang C, Zhou J, Jang HJ, Yoon SH, Kim JY, Lee SG, et al. Engineered heterologous FPP synthases-mediated Z, E-FPP synthesis in E. coli. Metab Eng. 2013;18:53–9.
18. Westfall PJ, Pitera DJ, Lenihan JR, Eng D, Woolard FX, Regentin R, et al. Production of amorphadiene in yeast, and its conversion to dihydroar-temisinic acid, precursor to the antimalarial agent artemisinin. Proc Natl Acad Sci USA. 2012;109(3):111–8.
19. Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, et al. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature. 2006;440(7086):940–3.
20. Zhou K, Qiao KJ, Edgar S, Stephanopoulos G. Distributing a metabolic pathway among a microbial consortium enhances production of natural products. Nat Biotechnol. 2015;33(4):377–83.
21. Melis A. Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci. 2009;177(4):272–80.
22. 2. Curr Opin Biotechnol. 2015;33:8–14.
23. Atsumi S, Higashide W, Liao JC. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat Biotechnol. 2009;27(12):1177–80.
24. Lan EI, Ro SY, Liao JC. Oxygen-tolerant coenzyme A-acylating aldehyde dehydrogenase facilitates efficient photosynthetic n-butanol biosynthesis in cyanobacteria. Energy Environ Sci. 2013;6(9):2672–81.
25. Oliver JW, Machado IM, Yoneda H, Atsumi S. Cyanobacterial conversion of carbon dioxide to 2,3-butanediol. Proc Natl Acad Sci USA. 2013;110(4):1249–54.
26. Bentley FK, Zurbriggen A, Melis A. Heterologous expression of the mevalonic acid pathway in cyanobacteria enhances endogenous carbon partitioning to isoprene. Mol Plant. 2014;7(1):71–86.
27. Davies FK, Work VH, Beliaev AS, Posewitz MC. Engineering limonene and bisabolene production in wild type and a glycogen-deficient mutant of synechococcus sp. pcc 7002. Front Bioeng Biotechnol. 2014;2:21.
28. Formighieri C, Melis A. Regulation of β-phellandrene synthase gene expression, recombinant protein accumulation, and monoterpene hydrocarbons production in Synechocystis transformants. Planta. 2014;240(2):309–24.
29. Englund E, Pattanaik B, Ubhayasekera SJ, Stensjo K, Bergquist J, Lindberg P. Production of squalene in Synechocystis sp. PCC 6803. PLoS ONE. 2014;9(3):e90270.
30. Kudoh K, Kawano Y, Hotta S, Sekine M, Watanabe T, Ihara M. Prerequisite for highly efficient isoprenoid production by cyanobacteria discovered through the over-expression of 1-deoxy-d-xylulose 5-phosphate synthase and carbon allocation analysis. J Biosci Bioeng. 2014;118(1):20–8.
31. Agger SA, Lopez-Gallego F, Hoye TR, Schmidt-Dannert C. Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120. J Bacteriol. 2008;190(18):6084–96.
32. Xu P, Gu Q, Wang W, Wong L, Bower AG, Collins CH, et al. Modular optimization of multi-gene pathways for fatty acids production in E. coli. Nat Commun. 2013;4:1409.
33. Chwa JW, Kim WJ, Sim SJ, Um Y, Woo HM. Engineering of a modular and synthetic phosphoketolase pathway for photosynthetic production of acetone from CO2 in Synechococcus elongatus PCC 7942 under light and aerobic condition. Plant Biotechnol J. 2016;14:1768–76.
34. Jin YS, Stephanopoulos G. Multi-dimensional gene target search for improving lycopene biosynthesis in Escherichia coli. Metab Eng. 2007;9(4):337–47.
35. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, et al. Programming cells by multiplex genome engineering and accelerated evolution. Nature. 2009;460(7257):894–8.
36. Zhang D, Jennings SM, Robinson GW, Poulter CD. Yeast squalene synthase: expression, purification, and characterization of soluble recombinant enzyme. Arch Biochem Biophys. 1993;304(1):133–43.
37. 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.
38. Leon R, Martin M, Vigara J, Vilchez C, Vega JM. Microalgae mediated pho-toproduction of beta-carotene in aqueous-organic two phase systems. Biomol Eng. 2003;20(4–6):177–82.
39. Redding-Johanson AM, Batth TS, Chan R, Krupa R, Szmidt HL, Adams PD, et al. Targeted proteomics for metabolic pathway optimization: application to terpene production. Metab Eng. 2011;13(2):194–203.
40. 2O. Green Chem. 2014;16(6):3175–85.
41. 2. J Biotechnol. 2014;185:1–7.
42. Miller B, Heuser T, Zimmer W. Functional involvement of a deoxy-d-xylu-lose 5-phosphate reductoisomerase gene harboring locus of Synechococcus leopoliensis in isoprenoid biosynthesis. FEBS Lett. 2000;481(3):221–6.
43. Xing S, Miao J, Li S, Qin G, Tang S, Li H, et al. Disruption of the 1-deoxy-d-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis. Cell Res. 2010;20(6):688–700.
44. Mahmoud SS, Croteau RB. Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc Natl Acad Sci USA. 2001;98(15):8915–20.
45. Borujeni AE, Channarasappa AS, Salis HM. Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites. Nucleic Acids Res. 2014;42(4):2646–59.
46. Torella JP, Ford TJ, Kim SN, Chen AM, Way JC, Silver PA. Tailored fatty acid synthesis via dynamic control of fatty acid elongation. Proc Natl Acad Sci USA. 2013;110(28):11290–5.
47. Murkin AS, Manning KA, Kholodar SA. Mechanism and inhibition of 1-deoxy-d-xylulose-5-phosphate reductoisomerase. Bioorg Chem. 2014;57:171–85.
48. Wang CW, Oh MK, Liao JC. Engineered isoprenoid pathway enhances astaxanthin production in Escherichia coli. Biotechnol Bioeng. 1999;62(2):235–41.
49. Yuan LZ, Rouviere PE, Larossa RA, Suh W. Chromosomal promoter replacement of the isoprenoid pathway for enhancing carotenoid production in E. coli. Metab Eng. 2006;8(1):79–90.
50. Reinsvold RE, Jinkerson RE, Radakovits R, Posewitz MC, Basu C. The production of the sesquiterpene β-caryophyllene in a transgenic strain of the cyanobacterium Synechocystis. J Plant Physiol. 2011;168(8):848–52.
51. Brunk E, George Kevin W, Alonso-Gutierrez J, Thompson M, Baidoo E, Wang G, et al. Characterizing strain variation in engineered E. coli using a multi-omics-based workflow. Cell Syst. 2016;2(5):335–46.
52. Lee PC, Petri R, Mijts BN, Watts KT, Schmidt-Dannert C. Directed evolution of Escherichia coli farnesyl diphosphate synthase (IspA) reveals novel structural determinants of chain length specificity. Metab Eng. 2005;7(1):18–26.
53. Dahl RH, Zhang F, Alonso-Gutierrez J, Baidoo E, Batth TS, Redding-Johanson AM, et al. Engineering dynamic pathway regulation using stress-response promoters. Nat Biotechnol. 2013;31(11):1039–46.
54. Li Y, Lin Y, Loughlin PC, Chen M. Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris—a filamentous cyanobacterium containing chlorophyll f. Front Plant Sci. 2014;5:67.
55. Formighieri C, Melis A. Sustainable heterologous production of terpene hydrocarbons in cyanobacteria. Photosynth Res. 2016. doi:10.1007/ s11120-016-0233-2.
56. 2. Energy Environ Sci. 2016;9(4):1400–11.
57. Formighieri C, Melis A. A phycocyanin phellandrene synthase fusion enhances recombinant protein expression and beta-phellandrene (monoterpene) hydrocarbons production in Synechocystis (cyanobacteria). Metab Eng. 2015;32:116–24.
58. 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(1):13–9.
59. Katabami A, Li L, Iwasaki M, Furubayashi M, Saito K, Umeno D. Production of squalene by squalene synthases and their truncated mutants in Escherichia coli. J Biosci Bioeng. 2015;119(2):165–71.
60. Zhang C, Chen X, Stephanopoulos G, Too HP. Efflux transporter engineering markedly improves amorphadiene production in Escherichia coli. Biotechnol Bioeng. 2016;113:1755–63.
61. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983;166(4):557–80.
62. Lee TS, Krupa RA, Zhang F, Hajimorad M, Holtz WJ, Prasad N, et al. BglBrick vectors and datasheets: a synthetic biology platform for gene expression. J Biol Eng. 2011;5:12.
63. Golden SS, Brusslan J, Haselkorn R. Genetic engineering of the cyanobacterial chromosome. Methods Enzymol. 1987;153:215–31.
64. Woo HM, Murray GW, Batth TS, Prasad N, Adams PD, Keasling JD, et al. Application of targeted proteomics and biological parts assembly in E. coli to optimize the biosynthesis of an anti-malarial drug precursor, amorpha-4,11-diene. Chem Eng Sci. 2013;103:21–8.
65. Jeffrey SW, Humphrey GF. New spectrophotometric equations for determining chlorophyll a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pfl. 1975;167(2):191–4.