Yeast factories for the production of aromatic compounds: from building blocks to plant secondary metabolites

Journal of Industrial Microbiology and Biotechnology

Volumn 43, Issue 11, 2016, Pages 1611-1624

  Suástegui, Miguel ^a,b   Shao, Zengyi ^a,b  

^a Iowa State University of Science and Technology   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Aromatic amino acids; Benzylisoquinoline alkaloids; Flavonoids; Metabolic engineering; Saccharomyces cerevisiae; Shikimic acid; Stilbenoids

Indexed keywords

ALKALOID DERIVATIVE; AROMATIC AMINO ACID; AROMATIC COMPOUND; BISBENZYLISOQUINOLINE DERIVATIVE; CARBON; COUMARIC ACID; CYTOCHROME P450 REDUCTASE; FLAVONOID; INDOLE ALKALOID; MELATONIN; MUCONIC ACID; NUTRACEUTICAL; PHENETHYL ALCOHOL; PHENYLALANINE; SHIKIMIC ACID; STILBENOID; TERPENE DERIVATIVE; TYROSINE; UNCLASSIFIED DRUG; VANILLIN; BENZYLISOQUINOLINE DERIVATIVE; SORBIC ACID;

ALLOSTERISM; AMINO ACID SYNTHESIS; CATALYST; METABOLIC ENGINEERING; NONHUMAN; REVIEW; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; DIETARY SUPPLEMENT; GENETICS; METABOLISM; PLANT; SECONDARY METABOLISM;

AMINO ACIDS, AROMATIC; BENZYLISOQUINOLINES; BIOSYNTHETIC PATHWAYS; DIETARY SUPPLEMENTS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; PLANTS; SACCHAROMYCES CEREVISIAE; SECONDARY METABOLISM; SHIKIMIC ACID; SORBIC ACID;

EID: 84984855496     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-016-1824-9     Document Type: Review

References (81)

1. Adelfo Escalante A, Carmona SB, Diaz Quiroz DC, Bolivar F (2014) Current perspectives on applications of shikimic and aminoshikimic acids in pharmaceutical chemistry. Res Rep Med Chem 4:35–46
2. Beaudoin GA, Facchini PJ (2014) Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta 240(1):19–32
3. Becker J, Wittmann C (2015) Advanced biotechnology: metabolically engineered cells for the bio-based production of chemicals and fuels, materials, and health-care products. Angew Chem Int Ed Engl 54(11):3328–3350
4. Becker JV, Armstrong GO, van der Merwe MJ, Lambrechts MG, Vivier MA, Pretorius IS (2003) Metabolic engineering of Saccharomyces cerevisiae for the synthesis of the wine-related antioxidant resveratrol. FEMS Yeast Res 4(1):79–85
5. Bender DA (2012) Amino acid metabolism, 3rd edn. Wiley-Blackwell, Chichester, West Sussex
6. Bermejo C, Haerizadeh F, Takanaga H, Chermak D, Frommer WB (2011) Optical sensors for measuring dynamic changes of cytosolic metabolite levels in yeast. Nat Protoc 6(11):1806–1817
7. Borodina I, Nielsen J (2014) Advances in metabolic engineering of yeast Saccharomyces cerevisiae for production of chemicals. Biotechnol J 9(5):609–620
8. Braus GH (1991) Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae: a model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol Rev 55(3):349–370
9. Brochado AR, Matos C, Møller BL, Hansen J, Mortensen UH, Patil KR (2010) Improved vanillin production in baker’s yeast through in silico design. Microb Cell Fact 9:84
10. Brown JF, Dawes IW (1990) Regulation of chorismate mutase in Saccharomyces cerevisiae. Mol Gen Genet 220(2):283–288
11. Brown S, Clastre M, Courdavault V, O’Connor SE (2015) De novo production of the plant-derived alkaloid strictosidine in yeast. Proc Natl Acad Sci USA 112(11):3205–3210
12. Buscemi N, Vandermeer B, Pandya R, Hooton N, Tjosvold L, Hartling L, Baker G, Vohra S, Klassen T (2004) Melatonin for treatment of sleep disorders. Evid Rep Technol Assess 108:1–7 (Summ)
13. Curran KA, Leavitt JM, Karim AS, Alper HS (2012) Metabolic engineering of muconic acid production in Saccharomyces cerevisiae. Metab Eng 15:55–66
14. Dai Z, Liu Y, Guo J, Huang L, Zhang X (2014) Yeast synthetic biology for high-value metabolites. FEMS Yeast Res 15(1):1–11
15. DeLoache WC, Russ ZN, Narcross L, Gonzales AM, Martin VJ, Dueber JE (2015) An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose. Nat Chem Biol 11(7):465–471
16. Du J, Yuan Y, Si T, Lian J, Zhao H (2012) Customized optimization of metabolic pathways by combinatorial transcriptional engineering. Nucleic Acids Res 40(18):e142
17. Elder M (2015) The global market for pain management drugs and services. Wellesley, MA
18. Etschmann MM, Bluemke W, Sell D, Schrader J (2002) Biotechnological production of 2-phenylethanol. Appl Microbiol Biotechnol 59(1):1–8
19. Facchini PJ, Bohlmann J, Covello PS, De Luca V, Mahadevan R, Page JE, Ro DK, Sensen CW, Storms R, Martin VJ (2012) Synthetic biosystems for the production of high-value plant metabolites. Trends Biotechnol 30(3):127–131
20. Farrow SC, Hagel JM, Beaudoin GA, Burns DC, Facchini PJ (2015) Stereochemical inversion of (S)-reticuline by a cytochrome P450 fusion in opium poppy. Nat Chem Biol 11(9):728–732
21. Fossati E, Ekins A, Narcross L, Zhu Y, Falgueyret JP, Beaudoin GA, Facchini PJ, Martin VJ (2014) Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae. Nat Commun 5:3283
22. Fukuda K, Watanabe M, Asano K (1990) Altered regulation of aromatic amino acid biosynthesis in β-phenylethyl alcohol overproducing mutants of sake yeast Saccharomyces cerevisiae. Agric Biol Chem 54(12):3151–3156
23. Fukuda K, Watanabe M, Asano K, Ouchi K, Takasawa S (1992) Molecular breeding of a sake yeast with a mutated ARO4 gene which causes both resistance to L-fluoro-Dl-phenylalanine and increased production of β-phenethyl alcohol. Ferment and Bioeng 73(5):366–369
24. Fukuda K, Watanabe M, Asano K, Ueda H, Ohta S (1990) Breeding of brewing yeast producing a large amount of β-phenylethyl alcohol and β-phenylethyl acetate. Agric Biol Chem 54(1):269–271
25. Galanie S, Thodey K, Trenchard IJ, Filsinger Interrante M, Smolke CD (2015) Complete biosynthesis of opioids in yeast. Science 349(6252):1095–1100
26. Geerlings A, Redondo F, Contin A, Memelink J, van der Heijden H, Verpoorte R (2001) Biotransformation of tryptamine and secologanin into plant terpenoid indole alkaloids by transgenic yeast. Appl Microbiol Biotechnol 56(3):420–424
27. Germann SM, Baallal Jacobsen SA, Schneider K, Harrison SJ, Jensen NB, Chen X, Stahlhut SG, Borodina I, Luo H, Zhu J, Maury J, Forster J (2015) Glucose-based microbial production of the hormone melatonin in yeast Saccharomyces cerevisiae. Biotechnol J. doi:10.1002/biot.201500143
28. Gobbi PG, Broglia C, Merli F, Dell’Olio M, Stelitano C, Iannitto E, Federico M, Berte R, Luisi D, Molica S, Cavalli C, Dezza L, Ascari E (2003) Vinblastine, bleomycin, and methotrexate chemotherapy plus irradiation for patients with early-stage, favorable Hodgkin lymphoma: the experience of the Gruppo Italiano Studio Linfomi. Cancer 98(11):2393–2401
29. Gold ND, Gowen CM, Lussier F-X, Cautha SC, Mahadevan R, Martin VJJ (2015) Metabolic engineering of a tyrosine-overproducing yeast platform using targeted metabolomics. Microb Cell Fact 14:73
30. Hagel JM, Facchini PJ (2013) Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world. Plant Cell Physiol 54(5):647–672
31. Hansen EH, Moller BL, Kock GR, Bunner CM, Kristensen C, Jensen OR, Okkels FT, Olsen CE, Motawia MS, Hansen J (2009) De novo biosynthesis of vanillin in fission yeast (Schizosaccharomyces pombe) and baker’s yeast (Saccharomyces cerevisiae). Appl Environ Microbiol 75(9):2765–2774
32. Hawkins KM, Smolke CD (2008) Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol 4(9):564–573
33. He L, Li JL, Zhang JJ, Su P, Zheng SL (2003) Microwave assisted synthesis of melatonin. Synth Comm 33(5):741–747
34. Heiskanen A, Coman V, Kostesha N, Sabourin D, Haslett N, Baronian K, Gorton L, Dufva M, Emnéus J (2013) Bioelectrochemical probing of intracellular redox processes in living yeast cells—application of redox polymer wiring in a microfluidic environment. Anal Bioanal Chem 405(11):3847–3858
35. Higashi Y, Smith TJ, Jez JM, Kutchan TM (2010) Crystallization and preliminary X-ray diffraction analysis of salutaridine reductase from the opium poppy Papaver somniferum. Acta Crystallogr Sect F Struct Biol Cryst Commun 66(Pt 2):163–166
36. Hinnebusch AG (1988) Mechanisms of gene regulation in the general control of amino acid biosynthesis in Saccharomyces cerevisiae. Microbiol Rev 52(2):248–273
37. Hinnebusch AG, Natarajan K (2002) Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot Cell 1(1):22
38. Jendresen CB, Stahlhut SG, Li M, Gaspar P, Siedler S, Forster J, Maury J, Borodina I, Nielsen AT (2015) Highly active and specific tyrosine ammonia-lyases from diverse origins enable enhanced production of aromatic compounds in bacteria and Saccharomyces cerevisiae. Appl Environ Microbiol 81(13):4458–4476
39. Jiang H, Morgan JA (2004) Optimization of an in vivo plant P450 monooxygenase system in Saccharomyces cerevisiae. Biotechnol Bioeng 85(2):130–137
40. Jiang H, Wood KV, Morgan JA (2005) Metabolic engineering of the phenylpropanoid pathway in Saccharomyces cerevisiae. Appl Environ Microbiol 71(6):2962–2969
41. Jones JA, Vernacchio VR, Sinkoe AL, Collins SM, Ibrahim MH, Lachance DM, Hahn J, Koffas MA (2016) Experimental and computational optimization of an Escherichia coli co-culture for the efficient production of flavonoids. Metab Eng 35:55–63
42. Jullesson D, David F, Pfleger B, Nielsen J (2015) Impact of synthetic biology and metabolic engineering on industrial production of fine chemicals. Biotechnol Adv 33(7):1395–1402
43. Kamei Y, Hayakawa T, Urata J, Uchiyama M, Shibui K, Kim K, Kudo Y, Okawa M (2000) Melatonin treatment for circadian rhythm sleep disorders. Psychiatry Clin Neurosci 54(3):381–382
44. Kim B, Cho BR, Hahn JS (2014) Metabolic engineering of Saccharomyces cerevisiae for the production of 2-phenylethanol via Ehrlich pathway. Biotechnol Bioeng 111(1):115–124
45. Koopman F, Beekwilder J, Crimi B, Van Houwelingen A, Hall Robert D, Bosch D, Van Maris Antonius J, Pronk Jack T, Daran JM (2012) De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae. Microb Cell Fact 11(1):155
46. Lee K, Hahn JS (2013) Interplay of Aro80 and GATA activators in regulation of genes for catabolism of aromatic amino acids in Saccharomyces cerevisiae. Mol Microbiol 88(6):1120–1134
47. Li M, Kildegaard KR, Chen Y, Rodriguez A, Borodina I, Nielsen J (2015) De novo production of resveratrol from glucose or ethanol by engineered Saccharomyces cerevisiae. Metab Eng 32:1–11
48. Lu R, Lu F, Chen J, Yu W, Huang Q, Zhang J, Xu J (2016) Production of diethyl terephthalate from biomass-derived muconic acid. Angew Chem Int Ed Engl 55(1):249–253
49. Luttik MAH, Vuralhan Z, Suir E, Braus GH, Pronk JT, Daran JM (2008) Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: quantification of metabolic impact. Metab Eng 10(3):141–153
50. Mannhaupt G, Stucka R, Pilz U, Schwarzlose C, Feldmann H (1989) Characterization of the prephenate dehydrogenase-encoding gene, TYR1, from Saccharomyces cerevisiae. Gene 85(2):303–311
51. Minami H, Kim JS, Ikezawa N, Takemura T, Katayama T, Kumagai H, Sato F (2008) Microbial production of plant benzylisoquinoline alkaloids. Proc Natl Acad Sci USA 105(21):7393–7398
52. Moxley JF, Jewett MC, Antoniewicz MR, Villas-Boas SG, Alper H, Wheeler RT, Tong L, Hinnebusch AG, Ideker T, Nielsen J, Stephanopoulos G (2009) Linking high-resolution metabolic flux phenotypes and transcriptional regulation in yeast modulated by the global regulator Gcn4p. Proc Natl Acad Sci USA 106(16):6477
53. Niu W, Draths KM, Frost JW (2002) Benzene-free synthesis of adipic acid. Biotechnol Prog 18(2):201–211
54. Oud B, Flores CL, Gancedo C, Zhang X, Trueheart J, Daran JM, Pronk JT, van Maris AJ (2012) An internal deletion in MTH1 enables growth on glucose of pyruvate-decarboxylase negative, non-fermentative Saccharomyces cerevisiae. Microb Cell Fact 11:131
55. Pandal N (2014) Global markets for flavors and fragrances. BCC Research. Wellesley, MA
56. Pasquali G, Porto DD, Fett-Neto AG (2006) Metabolic engineering of cell cultures versus whole plant complexity in production of bioactive monoterpene indole alkaloids: recent progress related to old dilemma. J Biosci Bioeng 101(4):287–296
57. Picataggio S, Beardslee T (2012) Biological methods for preparing adipic acid. Patent number US8241879 B2
58. Priefert H, Rabenhorst J, Steinbuchel A (2001) Biotechnological production of vanillin. Appl Microbiol Biotechnol 56(3–4):296–314
59. Ro DK, Ehlting J, Douglas CJ (2002) Cloning, functional expression, and subcellular localization of multiple NADPH-cytochrome P450 reductases from hybrid poplar. Plant Physiol 130(4):1837–1851
60. Rodriguez A, Kildegaard KR, Li M, Borodina I, Nielsen J (2015) Establishment of a yeast platform strain for production of p-coumaric acid through metabolic engineering of aromatic amino acid biosynthesis. Metab Eng 31:181–188
61. Rodriguez-Naranjo MI, Torija MJ, Mas A, Cantos-Villar E, Garcia-Parrilla Mdel C (2012) Production of melatonin by Saccharomyces strains under growth and fermentation conditions. J Pineal Res 53(3):219–224
62. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276(39):36566
63. Shin SY, Jung SM, Kim MD, Han NS, Seo JH (2012) Production of resveratrol from tyrosine in metabolically engineered Saccharomyces cerevisiae. Enzyme Microb Technol 51(4):211–216
64. Sonawane B, Bayliss D, Valcovic L, Chen C, Rodan B, Farland W (2000) Carcinogenic effects of benzene–a status update and research needs to improve risk assessments: US EPA perspective. Environmental Protection Agency. J Toxicol Environ Health A 61(5–6):471–472
65. Stark D, Kornmann H, Münch T, Sonnleitner B, Marison IW, Von Stockar U (2003) Novel type of in situ extraction: use of solvent containing microcapsules for the bioconversion of 2-phenylethanol from l-phenylalanine by Saccharomyces cerevisiae. Biotechnol Bioeng 83(4):376–385
66. Stark D, Münch T, Sonnleitner B, Marison IW, Stockar UV (2002) Extractive bioconversion of 2-phenylethanol from L-phenylalanine by Saccharomyces cerevisiae. Biotechnol Prog 18(3):514–523
67. Suástegui M, Guo W, Feng X, Shao Z (2016) Investigating strain dependency in the production of aromatic compounds in Saccharomyces cerevisiae. Biotechnol Bioeng. doi:10.1002/bit.26037
68. Suastegui M, Matthiesen JE, Carraher JM, Hernandez N, Rodriguez Quiroz N, Okerlund A, Cochran EW, Shao Z, Tessonnier JP (2016) Combining metabolic engineering and electrocatalysis: application to the production of polyamides from sugar. Angew Chem Int Ed Engl 55(7):2368–2373
69. Sun X, Lin Y, Yuan Q, Yan Y (2015) Precursor-directed biosynthesis of 5-hydroxytryptophan using metabolically engineered E. coli. ACS Synth Biol 4(5):554–558
70. Sydor T, Schaffer S, Boles E (2010) Considerable increase in resveratrol production by recombinant industrial yeast strains with use of rich medium. Appl Environ Microbiol 76(10):3361–3363
71. Szczebara FM, Chandelier C, Villeret C, Masurel A, Bourot S, Duport C, Blanchard S, Groisillier A, Testet E, Costaglioli P, Cauet G, Degryse E, Balbuena D, Winter J, Achstetter T, Spagnoli R, Pompon D, Dumas B (2003) Total biosynthesis of hydrocortisone from a simple carbon source in yeast. Nat Biotechnol 21(2):143–149
72. Trantas E, Panopoulos N, Ververidis F (2009) Metabolic engineering of the complete pathway leading to heterologous biosynthesis of various flavonoids and stilbenoids in Saccharomyces cerevisiae. Metab Eng 11(6):355–366
73. Trenchard IJ, Siddiqui MS, Thodey K, Smolke CD (2015) De novo production of the key branch point benzylisoquinoline alkaloid reticuline in yeast. Metab Eng 31:74–83
74. Vannelli T, Wei Qi W, Sweigard J, Gatenby AA, Sariaslani FS (2007) Production of p-hydroxycinnamic acid from glucose in Saccharomyces cerevisiae and Escherichia coli by expression of heterologous genes from plants and fungi. Metab Eng 9(2):142–151
75. Wang Y, Halls C, Zhang J, Matsuno M, Zhang Y, Yu O (2011) Stepwise increase of resveratrol biosynthesis in yeast Saccharomyces cerevisiae by metabolic engineering. Metab Eng 13(5):455–463
76. Winzer T, Kern M, King AJ, Larson TR, Teodor RI, Donninger SL, Li Y, Dowle AA, Cartwright J, Bates R, Ashford D, Thomas J, Walker C, Bowser TA, Graham IA (2015) Plant science. Morphinan biosynthesis in opium poppy requires a P450-oxidoreductase fusion protein. Science 349(6245):309–312
77. Zhang H, Pereira B, Li Z, Stephanopoulos G (2015) Engineering Escherichia coli coculture systems for the production of biochemical products. Proc Natl Acad Sci USA 112(27):8266–8271
78. Zhang J, Wu C, Sheng J, Feng X (2016) Molecular basis of 5-hydroxytryptophan synthesis in Saccharomyces cerevisiae. Mol Biosyst. doi:10.1039/c5mb00888c
79. Zhu C, Byers KJ, McCord RP, Shi Z, Berger MF, Newburger DE, Saulrieta K, Smith Z, Shah MV, Radhakrishnan M, Philippakis AA, Hu Y, De Masi F, Pacek M, Rolfs A, Murthy T, Labaer J, Bulyk ML (2009) High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19(4):556–566
80. Ziegler J, Brandt W, Geissler R, Facchini PJ (2009) Removal of substrate inhibition and increase in maximal velocity in the short chain dehydrogenase/reductase salutaridine reductase involved in morphine biosynthesis. J Biol Chem 284(39):26758–26767
81. Ziegler J, Facchini PJ, Geissler R, Schmidt J, Ammer C, Kramell R, Voigtlander S, Gesell A, Pienkny S, Brandt W (2009) Evolution of morphine biosynthesis in opium poppy. Phytochemistry 70(15–16):1696–1707