Abstract
As an important raw material for pharmaceutical, food and feed industry, highly efficient production of L-tryptophan by Escherichia coli has attracted a considerable attention. However, there are complicated and multiple layers of regulation networks in L-tryptophan biosynthetic pathway and thus have difficulty to rewrite the biosynthetic pathway for producing L-tryptophan with high efficiency in E. coli. This review summarizes the biosynthetic pathway of L-tryptophan and highlights the main regulatory mechanisms in E. coli. In addition, we discussed the latest metabolic engineering strategies achieved in E. coli to reconstruct the L-tryptophan biosynthetic pathway. Moreover, we also review a few strategies that can be used in E. coli to improve robustness and streamline of L-tryptophan high-producing strains. Lastly, we also propose the potential strategies to further increase L-tryptophan production by systematic metabolic engineering and synthetic biology techniques.
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Abbreviations
- TCA:
-
Tricarboxylic acid
- EMP:
-
Glycolytic pathway
- PP:
-
Pentose phosphate
- PTS:
-
Phosphotransferase system
- MDS:
-
Multiple-deletion series
- G6P:
-
Glucose-6-phosphate
- 6PGL:
-
6-Phosphogluconolactone
- 6PG:
-
6-Phosphogluconate
- Ru5P:
-
Ribulose-5-phosphate
- E4P:
-
Erythrose-4-phosphate
- F6P:
-
Fructose-6-phosphate
- GA3P:
-
Glyceraldehyde-3-phosphate
- 3-PG:
-
3-Phosophoglycerate
- PEP:
-
Phosphoenolpyruvate
- Pyr:
-
Pyruvate; Ace-CoA, acetyl-CoA
- ICit:
-
Isocitrate; α-KG, α-ketoglutarate
- Suc:
-
Succinate; Mal, malate
- OAA:
-
Oxaloacetate
- Gln:
-
L-glutamine
- Ser:
-
L-serine
- Trp:
-
L-tryptophan
- Glu:
-
L-glutamate
- PRPP:
-
Phosphoribosyl pyrophosphate
- DAHP:
-
3-Deoxy-d-arobino-heptulosonate 7-phosphate
- PRA:
-
Anthranilate-5-phosphoribosyl pyrophosphate
- InGP:
-
InG phosphate
- CDRP:
-
1-(O-carboxyphenyl amino) 1-deoxyribulose 5-phosphate
References
Abdel-Hamid AM, Attwood MM, Guest JR (2001) Pyruvate oxidase contributes to the aerobic growth efficiency of Escherichia Coli. Microbiol-Sgm 147:1483–1498. https://doi.org/10.1099/00221287-147-6-1483
Aiba S, Tsunekawa H, Imanaka T (1982) New approach to tryptophan production by Escherichia coli: genetic manipulation of composite plasmids in vitro. Appl Environ Microbiol 43:289–297. https://doi.org/10.1128/aem.43.2.289-297.1982
Airich LG, Tsyrenzhapova IS, Vorontsova OV, Feofanov AV, Doroshenko VG, Mashko SV (2010) Membrane topology analysis of the Escherichia coli aromatic amino acid efflux protein YddG. J Mol Microbiol Biotechnol 19:189–197. https://doi.org/10.1159/000320699
Audit C, Anagnostopoulos C (1973) Genetic studies relating to the production of transformed clones diploid in the tryptophan region of the Bacillus subtilis genome. J Bacteriol 114:18–27. https://doi.org/10.1128/jb.114.1.18-27.1973
Azuma S, Tsunekawa H, Okabe M, Okamoto R, Aiba S (1993) Hyper-production of L-tryptophan via fermentation with crystallization. Appl Microbiol Biot 39:471–476. https://doi.org/10.1007/Bf00205035
Bai Y, Lang EJM, Nazmi AR, Parker EJ (2019) Domain cross-talk within a bifunctional enzyme provides catalytic and allosteric functionality in the biosynthesis of aromatic amino acids. J Biol Chem 294:4828–4842. https://doi.org/10.1074/jbc.RA118.005220
Baker TI, Crawford IP (1966) Anthranilate synthetase. Partial purification and some kinetic studies on the enzyme from Escherichia Coli. J Biol Chem 241:5577–5584
Basan M, Hui S, Okano H, Zhang ZG, Shen Y, Williamson JR, Hwa T (2015) Overflow metabolism in Escherichia coli results from efficient proteome allocation. Nature 528:99–104. https://doi.org/10.1038/nature15765
Bassalo MC et al (2016) Rapid and efficient one-step metabolic pathway integration in E. coli. ACS Synth Biol 5:561–568. https://doi.org/10.1021/acssynbio.5b00187
Becker J, Klopprogge C, Zelder O, Heinzle E, Wittmann C (2005) Amplified expression of fructose 1,6-bisphosphatase in Corynebacterium glutamicum increases in vivo flux through the pentose phosphate pathway and lysine production on different carbon sources. Appl Environ Microb 71:8587–8596. https://doi.org/10.1128/Aem.71.12.8587-8596.2005
Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5:593–599. https://doi.org/10.1038/nchembio.186
Bernal V, Castano-Cerezo S, Canovas M (2016) Acetate metabolism regulation in Escherichia coli: carbon overflow, pathogenicity, and beyond. Appl Microbiol Biot 100:8985–9001. https://doi.org/10.1007/s00253-016-7832-x
Berry A (1996) Improving production of aromatic compounds in Escherichia coli by metabolic engineering. Trends Biotechnol 14:250–256. https://doi.org/10.1016/0167-7799(96)10033-0
Bertrand K, Yanofsky C (1976) Regulation of transcription termination in the leader region of the tryptophan operon of Escherichia coli involves tryptophan or its metabolic product. J Mol Biol 103:339–349. https://doi.org/10.1016/0022-2836(76)90316-8
Bongaerts J, Kramer M, Muller U, Raeven L, Wubbolts M (2001) Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab Eng 3:289–300. https://doi.org/10.1006/mben.2001.0196
Burkovski A, Kramer R (2002) Bacterial amino acid transport proteins: occurrence, functions, and significance for biotechnological applications. Appl Microbiol Biot 58:265–274. https://doi.org/10.1007/s00253-001-0869-4
Caligiuri MG, Bauerle R (1991) Subunit communication in the anthranilate synthase complex from Salmonella typhimurium. Science 252:1845–1848. https://doi.org/10.1126/science.2063197
Carvalho SM, Marques J, Romao CC, Saraiva LM (2019) Metabolomics of Escherichia coli treated with the antimicrobial carbon monoxide-releasing molecule CORM-3 reveals tricarboxylic acid Cycle as major target. Antimicrob Agents Chemother 63(10):e00643-19. https://doi.org/10.1128/AAC.00643-19
Castano-Cerezo S, Pastor JM, Renilla S, Bernal V, Iborra JL, Canovas M (2009) An insight into the role of phosphotransacetylase (pta) and the acetate/acetyl-CoA node in Escherichia coli. Microb Cell Fact 8:54–72. https://doi.org/10.1186/1475-2859-8-54
Castano-Cerezo S et al (2014) Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli. Mol Syst Biol 10(11):762–776. https://doi.org/10.15252/msb.20145227
Chakrabarti AC, Deamer DW (1992) Permeability of lipid bilayers to amino acids and phosphate. Biochem Biophys Acta 1111:171–177. https://doi.org/10.1016/0005-2736(92)90308-9
Chan EC, Tsai HL, Chen SL, Mou DG (1993) Amplification of the tryptophan operon gene in Escherichia Coli chromosome to increase L-Tryptophan biosynthesis. Appl Microbiol Biot 40:301–305
Chen L, Zeng AP (2017) Rational design and metabolic analysis of Escherichia Coli for effective production of L-Tryptophan at high concentration. Appl Microbiol Biot 101:559–568. https://doi.org/10.1007/s00253-016-7772-5
Chen YY, Stabryla L, Wei N (2016) Improved acetic acid resistance in Saccharomyces cerevisiae by overexpression of the WHI2 gene identified through inverse metabolic engineering. Appl Environ Microb 82:2156–2166. https://doi.org/10.1128/Aem.03718-15
Chen L, Chen ML, Ma CW, Zeng AP (2018) Discovery of feed-forward regulation in L-tryptophan biosynthesis and its use in metabolic engineering of E. coli for efficient tryptophan bioproduction. Metab Eng 47:434–444. https://doi.org/10.1016/j.ymben.2018.05.001
Chen YY, Liu YF, Ding DQ, Cong LN, Zhang DW (2018) Rational design and analysis of an Escherichia Coli strain for high-efficiency tryptophan production. J Ind Microbiol Biot 45:357–367. https://doi.org/10.1007/s10295-018-2020-x
Cho BK, Federowicz S, Park YS, Zengler K, Palsson BO (2012) Deciphering the transcriptional regulatory logic of amino acid metabolism. Nat Chem Biol 8:65–71. https://doi.org/10.1038/nchembio.710
Choe D et al (2019) Adaptive laboratory evolution of a genome-reduced Escherichia Coli. Nat Commun 10(1):935–948. https://doi.org/10.1038/s41467-019-08888-6
Chye ML, Guest JR, Pittard J (1986) Cloning of the aroP gene and identification of its product in Escherichia coli K-12. J Bacteriol 167:749–753. https://doi.org/10.1128/jb.167.2.749-753.1986
Creighton TE, Yanofsky C (1966) Indole-3-glycerol phosphate synthetase of Escherichia coli, an enzyme of the tryptophan operon. J Biol Chem 241:4616–4624
Csorgo B, Feher T, Timar E, Blattner FR, Posfai G (2012) Low-mutation-rate, reduced-genome Escherichia coli: an improved host for faithful maintenance of engineered genetic constructs. Microb Cell Fact. https://doi.org/10.1186/1475-2859-11-11
Cui YY, Ling C, Zhang YY, Huang J, Liu JZ (2014) Production of shikimic acid from Escherichia coli through chemically inducible chromosomal evolution and cofactor metabolic engineering. Microb Cell Fact 13:21–31. https://doi.org/10.1186/1475-2859-13-21
Dopheide TA, Crewther P, Davidson BE (1972) Chorismate mutase-prephenate dehydratase from Escherichia coli K-12. II. Kinetic Properties. J Biol Chem 247:4447–4452
Doroshenko V, Airich L, Vitushkina M, Kolokolova A, Livshits V, Mashko S (2007) YddG from Escherichia coli promotes export of aromatic amino acids. FEMS Microbiol Lett 275:312–318. https://doi.org/10.1111/j.1574-6968.2007.00894.x
Du LH, Zhang Z, Xu QY, Chen N (2019a) Central metabolic pathway modification to improve L-Tryptophan production in Escherichia Coli. Bioengineered 10:59–70. https://doi.org/10.1080/21655979.2019.1592417
Du LH, Zhang Z, Xu QY, Chen N (2019b) New strategy for removing acetic acid as a by-product during L-Tryptophan production. Biotechnol Biotec Eq 33:1471–1480. https://doi.org/10.1080/13102818.2019.1674692
Fisher MA, Boyarskiy S, Yamada MR, Kong NW, Bauer S, Tullman-Ercek D (2014) Enhancing tolerance to short-chain alcohols by engineering the Escherichia Coli AcrB efflux pump to secrete the non-native substrate n-Butanol. ACS Synth Biol 3:30–40. https://doi.org/10.1021/sb400065q
Flores N, Xiao J, Berry A, Bolivar F, Valle F (1996) Pathway engineering for the production of aromatic compounds in Escherichia coli. Nat Biotechnol 14:620–623. https://doi.org/10.1038/nbt0596-620
Gaimster H, Summers D (2015) Regulation of indole signalling during the transition of E. coli from exponential to stationary phase. PLoS One 10(9):e0136691. https://doi.org/10.1371/journal.pone.0136691
Gall DL, Ralph J, Donohue TJ, Noguera DR (2017) Biochemical transformation of lignin for deriving valued commodities from lignocellulose Curr Opin. Biotech 45:120–126. https://doi.org/10.1016/j.copbio.2017.02.015
Gama-Castro S et al (2011) RegulonDB version 7.0: transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units). Nucleic Acids Res 39:D98–D105. https://doi.org/10.1093/nar/gkq1110
Ger YM, Chen SL, Chiang HJ, Shiuan D (1994) A single Ser-180 mutation desensitizes feedback inhibition of the phenylalanine-sensitive 3-deoxy-D-arabino-heptulosonate 7-phosphate (DAHP) synthetase in Escherichia coli. J Biochem-Tokyo 116:986–990. https://doi.org/10.1093/oxfordjournals.jbchem.a124657
Gibson F, Jones MJ, Teltscher H (1955) Synthesis of indole and anthranilic acid by mutants of Escherichia coli. Nature 175:853–854. https://doi.org/10.1038/175853a0
Gimenez R, Nunez MF, Badia J, Aguilar J, Baldoma L (2003) The gene yjcG, cotranscribed with the gene acs, encodes an acetate permease in Escherichia coli. J Bacteriol 185:6448–6455. https://doi.org/10.1128/Jb.185.21.6448-6455.2003
Gish K, Yanofsky C (1995) Evidence suggesting cis action by the TnaC leader peptide in regulating transcription attenuation in the tryptophanase operon of Escherichia coli. J Bacteriol 177:7245–7254. https://doi.org/10.1128/jb.177.24.7245-7254.1995
Gong ZW, Nielsen J, Zhou YJJ (2017) Engineering robustness of microbial cell factories. Biotechnol J 12(10):1700014–2170022. https://doi.org/10.1002/biot.201700014
Gottardi M, Reifenrath M, Boles E, Tripp J (2017) Pathway engineering for the production of heterologous aromatic chemicals and their derivatives in Saccharomyces cerevisiae: bioconversion from glucose. FEMS Yeast Res 17(4):1–11. https://doi.org/10.1093/femsyr/fox035
Gu PF, Yang F, Kang JH, Wang Q, Qi QS (2012) One-step of tryptophan attenuator inactivation and promoter swapping to improve the production of L-tryptophan in Escherichia coli. Microb Cell Fact 11:30–38. https://doi.org/10.1186/1475-2859-11-30
Gu P, Yang F, Li F, Liang Q, Qi Q (2013) Knocking out analysis of tryptophan permeases in Escherichia coli for improving L-tryptophan production. Appl Microbiol Biotechnol 97:6677–6683. https://doi.org/10.1007/s00253-013-4988-5
Gu PF, Yang F, Su TY, Wang Q, Liang QF, Qi QS (2015) A rapid and reliable strategy for chromosomal integration of gene(s) with multiple copies. Sci Rep 5:9684. https://doi.org/10.1038/srep09684
Guan NZ, Liu L (2020) Microbial response to acid stress: mechanisms and applications. Appl Microbiol Biot 104:51–65. https://doi.org/10.1007/s00253-019-10226-1
Gunsalus RP, Yanofsky C (1980) Nucleotide sequence and expression of Escherichia coli trpR, the structural gene for the trp aporepressor. Proc Natl Acad Sci USA 77:7117–7121. https://doi.org/10.1073/pnas.77.12.7117
Hille F, Richter H, Wong SP, Bratovic M, Ressel S, Charpentier E (2018) The biology of CRISPR-Cas: backward and forward. Cell 172:1239–1259. https://doi.org/10.1016/j.cell.2017.11.032
Hossain GS, Saini M, Miyake R, Ling H, Chang MW (2020) Genetic biosensor design for natural product biosynthesis in microorganisms. Trends Biotechnol 38:797–810. https://doi.org/10.1016/j.tibtech.2020.03.013
Hu YD, Liu XB, Ren ATM, Gu JD, Cao B (2019) Optogenetic modulation of a catalytic biofilm for the biotransformation of indole into tryptophan. Chemsuschem 12:5142–5148. https://doi.org/10.1002/cssc.201902413
Hudson GS, Howlett GJ, Davidson BE (1983) The binding of tyrosine and NAD+ to chorismate mutase/prephenate dehydrogenase from Escherichia coli K12 and the effects of these ligands on the activity and self-association of the enzyme. Analysis in Terms of a Model. J Biol Chem 258:3114–3120
Ikeda M (2006) Towards bacterial strains overproducing L-Tryptophan and other aromatics by metabolic engineering. Appl Microbiol Biot 69:615–626. https://doi.org/10.1007/s00253-005-0252-y
Ikeda M, Katsumata R (1999) Hyperproduction of tryptophan by Corynebacterium Glutamicum with the modified pentose phosphate pathway. Appl Environ Microb 65:2497–2502
Ito J, Yanofsky C (1966) The nature of the anthranilic acid synthetase complex of Escherichia coli. J Biol Chem 241:4112–4114
Jiang T, Li CY, Teng YX, Zhang RH, Yan YJ (2020) Recent advances in improving metabolic robustness of microbial cell factories Curr Opin. Biotech 66:69–77. https://doi.org/10.1016/j.copbio.2020.06.006
Jing K, Tang YW, Yao CY, del Rio-Chanona EA, Ling XP, Zhang DD (2018) Overproduction of L-tryptophan via simultaneous feed of glucose and anthranilic acid from recombinant Escherichia coli W3110: Kinetic modeling and process scale-up. Biotechnol Bioeng 115:371–381. https://doi.org/10.1002/bit.26398
Juhas M (2016) On the road to synthetic life: the minimal cell and genome-scale engineering. Crit Rev Biotechnol 36:416–423. https://doi.org/10.3109/07388551.2014.989423
Juhas M, Eberl L, Church GM (2012) Essential genes as antimicrobial targets and cornerstones of synthetic biology. Trends Biotechnol 30:601–607. https://doi.org/10.1016/j.tibtech.2012.08.002
Khan F, Tabassum N, Pham DTN, Oloketuyi SF, Kim YM (2020) Molecules involved in motility regulation in Escherichia coli cells: a review. Biofouling 36:889–908. https://doi.org/10.1080/08927014.2020.1826939
Kikuchi Y, Tsujimoto K, Kurahashi O (1997) Mutational analysis of the feedback sites of phenylalanine-sensitive 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase of Escherichia coli. Appl Environ Microb 63:761–762. https://doi.org/10.1128/Aem.63.2.761-762.1997
Kim J, Darlington A, Salvador M, Utrilla J, Jimenez JI (2020) Trade-offs between gene expression, growth and phenotypic diversity in microbial populations. Curr Opin Biotech 62:29–37. https://doi.org/10.1016/j.copbio.2019.08.004
Kramer R (1994) Systems and mechanisms of amino acid uptake and excretion in prokaryotes. Arch Microbiol 162:1–13
Kubota T, Tanaka Y, Takemoto N, Watanabe A, Hiraga K, Inui M, Yukawa H (2014) Chorismate-dependent transcriptional regulation of quinate/shikimate utilization genes by LysR-type transcriptional regulator QsuR in Corynebacterium glutamicum: carbon flow control at metabolic branch point. Mol Microbiol 92:356–368. https://doi.org/10.1111/mmi.12560
Kuhlman TE, Cox EC (2010) Site-specific chromosomal integration of large synthetic constructs. Nucleic Acids Res 38(6):e92. https://doi.org/10.1093/nar/gkp1193
Kumari S, Tishel R, Eisenbach M, Wolfe AJ (1995) Cloning, characterization, and functional expression of acs, the gene which encodes acetyl coenzyme. A synthetase in Escherichia coli. J Bacteriol 177:2878–2886. https://doi.org/10.1128/jb.177.10.2878-2886.1995
Larson MH, Gilbert LA, Wang XW, Lim WA, Weissman JS, Qi LS (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8:2180–2196. https://doi.org/10.1038/nprot.2013.132
Lawley B, Pittard AJ (1994) Regulation of Arol expression by Tyrr protein and Trp repressor in Escherichia coli K-12. J Bacteriol 176:6921–6930. https://doi.org/10.1128/Jb.176.22.6921-6930.1994
Lee SY (1996) High cell-density culture of Escherichia coli. Trends Biotechnol 14:98–105. https://doi.org/10.1016/0167-7799(96)80930-9
Lee JH, Lee J (2010) Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34:426–444. https://doi.org/10.1111/j.1574-6976.2009.00204.x
Lee JH, Wendisch VF (2017a) Biotechnological production of aromatic compounds of the extended shikimate pathway from renewable biomass. J Biotechnol 257:211–221. https://doi.org/10.1016/j.jbiotec.2016.11.016
Lee JH, Wendisch VF (2017b) Production of amino acids - Genetic and metabolic engineering approaches. Bioresource Technol 245:1575–1587. https://doi.org/10.1016/j.biortech.2017.05.065
Lee JH, Sung BH, Kim MS, Blattner FR, Yoon BH, Kim JH, Kim SC (2009) Metabolic engineering of a reduced-genome strain of Escherichia coli for L-threonine production. Microb Cell Fact 8:2–12. https://doi.org/10.1186/1475-2859-8-2
Lee JH, Jung SC, Bui LM, Kang KH, Song JJ, Kim SC (2013) Improved production of L-Threonine in Escherichia Coli by use of a DNA scaffold system. Appl Environ Microb 79:774–782. https://doi.org/10.1128/Aem.02578-12
Lee MY, Hung WP, Tsai SH (2017) Improvement of shikimic acid production in Escherichia coli with growth phase-dependent regulation in the biosynthetic pathway from glycerol WorldJ Microbiol. Biotechnol 33(2):25–32. https://doi.org/10.1007/s11274-016-2192-3
Li G, Young KD (2013) Indole production by the tryptophanase TnaA in Escherichia Coli is determined by the amount of exogenous tryptophan. Microbiol-SGM 159:402–410. https://doi.org/10.1099/mic.0.064139-0
Li Y, Chen GK, Tong XW, Zhang HT, Liu XG, Liu YH, Lu FP (2012) Construction of Escherichia coli strains producing L-serine from glucose. Biotechnol Lett 34:1525–1530. https://doi.org/10.1007/s10529-012-0937-0
Li L, Liu XC, Wei KK, Lu YH, Jiang WH (2019) Synthetic biology approaches for chromosomal integration of genes and pathways in industrial microbial systems. Biotechnol Adv 37:730–745. https://doi.org/10.1016/j.biotechadv.2019.04.002
Li Z, Ding D, Wang H, Liu L, Fang H, Chen T, Zhang D (2020) Engineering Escherichia coli to improve tryptophan production via genetic manipulation of precursor and cofactor pathways Synth Syst. Biotechnol 5:200–205. https://doi.org/10.1016/j.synbio.2020.06.009
Lieder S, Nikel PI, de Lorenzo V, Takors R (2015) Genome reduction boosts heterologous gene expression in Pseudomonas putida. Microb Cell Fact 14:23–36. https://doi.org/10.1186/s12934-015-0207-7
Liu Q, Cheng Y, Xie X, Xu Q, Chen N (2012) Modification of tryptophan transport system and its impact on production of L-tryptophan in Escherichia coli. Bioresour Technol 114:549–554. https://doi.org/10.1016/j.biortech.2012.02.088
Liu SP, Liu RX, Xiao MR, Zhang L, Ding ZY, Gu ZH, Shi GY (2014) A systems level engineered E. coli capable of efficiently producing L-phenylalanine. Process Biochem 49:751–757. https://doi.org/10.1016/j.procbio.2014.01.001
Liu LN, Duan XG, Wu J (2016a) L-Tryptophan production in Escherichia Coli improved by weakening the Pta-AckA pathway. PLoS One 11(6):e0158200. https://doi.org/10.1371/journal.pone.0158200
Liu XL, Lin J, Hu HF, Zhou B, Zhu BQ (2016b) Site-specific integration and constitutive expression of key genes into Escherichia Coli chromosome increases shikimic acid yields. Enzyme Microb Tech 82:96–104. https://doi.org/10.1016/j.enzmictec.2015.08.018
Liu LN, Chen S, Wu J (2017) Phosphoenolpyruvate:glucose phosphotransferase system modification increases the conversion rate during L-tryptophan production in Escherichia coli. J Ind Microbiol Biot 44:1385–1395. https://doi.org/10.1007/s10295-017-1959-3
Liu YF, Xu YR, Ding DQ, Wen JP, Zhu BW, Zhang DW (2018) Genetic engineering of Escherichia coli to improve L-phenylalanine production. BMC Biotechnol 18(1):5–16. https://doi.org/10.1186/s12896-018-0418-1
Liu LN, Bilal M, Luo HZ, Zhao YP, Iqbal HMN (2019) Metabolic engineering and fermentation process strategies for L-Tryptophan production by Escherichia Coli. Processes 36(2):e2944. https://doi.org/10.3390/pr7040213
Liu X, Niu H, Huang Z, Li Q, Gu P (2020) Construction of a switchable synthetic Escherichia coli for aromatic amino acids by a tunable switch. J Ind Microbiol Biotechnol 47:233–242. https://doi.org/10.1007/s10295-020-02262-y
Long CP, Antoniewicz MR (2019) Metabolic flux responses to deletion of 20 core enzymes reveal flexibility and limits of E. coli metabolism. Metab Eng 55:249–257. https://doi.org/10.1016/j.ymben.2019.08.003
Lynch JH, Dudareva N (2020) Aromatic amino acids: A complex network ripe for future exploration. Trends Plant Sci 25:670–681. https://doi.org/10.1016/j.tplants.2020.02.005
Mascarenhas D, Ashworth DJ, Chen CS (1991) Deletion of Pgi alters tryptophan biosynthesis in a genetically engineered strain of Escherichia Coli. Appl Environ Microb 57:2995–2999. https://doi.org/10.1128/Aem.57.10.2995-2999.1991
McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10:13–26. https://doi.org/10.1038/nrmicro2670
Na D, Yoo SM, Chung H, Park H, Park JH, Lee SY (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 31:170–174. https://doi.org/10.1038/nbt.2461
Nichols BP, Miozzari GF, van Cleemput M, Bennett GN, Yanofsky C (1980) Nucleotide sequences of the trpG regions of Escherichia coli, Shigella dysenteriae, Salmonella typhimurium and Serratia marcescens. J Mol Biol 142:503–517. https://doi.org/10.1016/0022-2836(80)90260-0
Niu H, Li RR, Wu J, Cai ZH, Yang DX, Gu PF, Li Q (2018) Production of succinate by recombinant Escherichia coli using acetate as the sole carbon source. 3 Biotech 8(10):421. https://doi.org/10.1007/s13205-018-1456-z
Niu H, Li RR, Liang QF, Qi QS, Li Q, Gu PF (2019) Metabolic engineering for improving L-Tryptophan production in Escherichia Coli. J Ind Microbiol Biot 46:55–65. https://doi.org/10.1007/s10295-018-2106-5
Ogino T, Garner C, Markley JL, Herrmann KM (1982) Biosynthesis of aromatic compounds: 13C NMR spectroscopy of whole Escherichia coli cells. Proc Natl Acad Sci USA 79:5828–5832. https://doi.org/10.1073/pnas.79.19.5828
Ou BM, Garcia C, Wang YJ, Zhang WP, Zhu GQ (2018) Techniques for chromosomal integration and expression optimization in Escherichia coli. Biotechnol Bioeng 115:2467–2478. https://doi.org/10.1002/bit.26790
Panichkin VB, Livshits VA, Biryukova IV, Mashko SV (2016) Metabolic engineering of Escherichia Coli for L-Tryptophan production. Appl Biochem Microb 52:783–809. https://doi.org/10.1134/S0003683816090052
Park JH, Lee SY (2008) Towards systems metabolic engineering of microorganisms for amino acid production Curr Opin. Biotech 19:454–460. https://doi.org/10.1016/j.copbio.2008.08.007
Park JH, Lee KH, Kim TY, Lee SY (2007) Metabolic engineering of Escherichia coli for the production of L-valine based on transcriptome analysis and in silico gene knockout simulation. Proc Natl Acad Sci USA 104:7797–7802. https://doi.org/10.1073/pnas.0702609104
Park MK, Lee SH, Yang KS, Jung SC, Lee JH, Kim SC (2014) Enhancing recombinant protein production with an Escherichia Coli host strain lacking insertion sequences. Appl Microbiol Biot 98:6701–6713. https://doi.org/10.1007/s00253-014-5739-y
Phue JN, Shiloach J (2004) Transcription levels of key metabolic genes are the cause for different glucose utilization pathways in E. coli B (BL21) and E. coli K (JM109). J Biotechnol 109:21–30. https://doi.org/10.1016/j.jbiotec.2003.10.038
Phue JN, Noronha SB, Hattacharyya R, Wolfe AJ, Shiloach J (2005) Glucose metabolism at high density growth of E. coli B and E. coli K: Differences in metabolic pathways are responsible for efficient glucose utilization in E. coli B as determined by microarrays and northern blot analyses. Biotechnol Bioeng 90:805–820. https://doi.org/10.1002/bit.20478
Pinhal S, Ropers D, Geiselmann J, de Jong H (2019) Acetate metabolism and the inhibition of bacterial growth by acetate. J Bacteriol 201(13):e00147-e219. https://doi.org/10.1128/JB.00147-19
Platt T, Yanofsky C (1975) An intercistronic region and ribosome-binding site in bacterial messenger RNA. Proc Natl Acad Sci USA 72:2399–2403. https://doi.org/10.1073/pnas.72.6.2399
Polen T, Kramer M, Bongaerts J, Wubbolts M, Wendisch VF (2005) The global gene expression response of Escherichia coli to L-phenylalanine. J Biotechnol 115:221–237. https://doi.org/10.1016/j.jbiotec.2004.08.017
Pontrelli S, Chiu TY, Lan EI, Chen FYH, Chang PC, Liao JC (2018) Escherichia coli as a host for metabolic engineering. Metab Eng 50:16–46. https://doi.org/10.1016/j.ymben.2018.04.008
Posfai G et al (2006) Emergent properties of reduced-genome Escherichia Coli. Science 312:1044–1046. https://doi.org/10.1126/science.1126439
Rodrigues AL et al (2013) Systems metabolic engineering of Escherichia coli for production of the antitumor drugs violacein and deoxyviolacein. Metab Eng 20:29–41. https://doi.org/10.1016/j.ymben.2013.08.004
Rodrigues AL, Becker J, Lima AODS, Porto LM, Wittmann C (2014) Systems metabolic engineering of Escherichia coli for gram scale production of the antitumor drug deoxyviolacein from glycerol. Biotechnol Bioeng 111:2280–2289. https://doi.org/10.1002/bit.25297
Santos CNS, Regitsky DD, Yoshikuni Y (2013) Implementation of stable and complex biological systems through recombinase-assisted genome engineering. Nat Commun 4:2503–2512. https://doi.org/10.1038/ncomms3503
Sarsero JP, Pittard AJ (1991) Molecular analysis of the Tyrr protein-mediated activation of Mtr gene expression in Escherichia coli K-12. J Bacteriol 173:7701–7704. https://doi.org/10.1128/jb.173.23.7701-7704.1991
Sarsero JP, Wookey PJ, Pittard AJ (1991) Regulation of expression of the Escherichia coli K-12 mtr gene by TyrR protein and Trp repressor. J Bacteriol 173:4133–4143. https://doi.org/10.1128/jb.173.13.4133-4143.1991
Seong W et al (2020) Adaptive laboratory evolution of Escherichia coli lacking cellular byproduct formation for enhanced acetate utilization through compensatory ATP consumption. Metab Eng 62:249–259. https://doi.org/10.1016/j.ymben.2020.09.005
Shen T, Liu Q, Xie XX, Xu QY, Chen N (2012) Improved production of tryptophan in genetically engineered Escherichia coli with TktA and PpsA overexpression. J Biomed Biotechnol 2012:605219. https://doi.org/10.1155/2012/605219
Sprenger GA (2007) From scratch to value: engineering Escherichia coli wild type cells to the production of L-phenylalanine and other fine chemicals derived from chorismate. Appl Microbiol Biotechnol 75:739–749. https://doi.org/10.1007/s00253-007-0931-y
Steiger MG, Rassinger A, Mattanovich D, Sauer M (2019) Engineering of the citrate exporter protein enables high citric acid production in Aspergillus niger. Metab Eng 52:224–231. https://doi.org/10.1016/j.ymben.2018.12.004
Stewart V, Yanofsky C (1986) Role of leader peptide synthesis in tryptophanase operon expression in Escherichia coli K-12. J Bacteriol 167:383–386. https://doi.org/10.1128/jb.167.1.383-386.1986
Tao H, Bausch C, Richmond C, Blattner FR, Conway T (1999) Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media. J Bacteriol 181:6425–6440. https://doi.org/10.1128/Jb.181.20.6425-6440.1999
Terol GL, Gallego-Jara J, Martinez RAS, Diaz MC, Puente TD (2019) Engineering protein production by rationally choosing a carbon and nitrogen source using E. coli BL21 acetate metabolism knockout strains. Microb Cell Fact 18(1):151–169. https://doi.org/10.1186/s12934-019-1202-1
Tovilla-Coutino DB, Momany C, Eiteman MA (2020) Engineered citrate synthase alters acetate accumulation in Escherichia coli. Metab Eng 61:171–180. https://doi.org/10.1016/j.ymben.2020.06.006
Trondle J, Trachtmann N, Sprenger GA, Weuster-Botz D (2018) Fed-batch production of L-tryptophan from glycerol using recombinant Escherichia coli. Biotechnol Bioeng 115:2881–2892. https://doi.org/10.1002/bit.26834
Trondle J, Schoppel K, Bleidt A, Trachtmann N, Sprenger GA, Weuster-Botz D (2020) Metabolic control analysis of L-tryptophan production with Escherichia coli based on data from short-term perturbation experiments. J Biotechnol 307:15–28. https://doi.org/10.1016/j.jbiotec.2019.10.009
Tsuchiya H et al (2016) Structural basis for amino acid export by DMT superfamily transporter YddG. Nature 534(7607):417–420. https://doi.org/10.1038/nature17991
Tyo KEJ, Ajikumar PK, Stephanopoulos G (2009) Stabilized gene duplication enables long-term selection-free heterologous pathway expression. Nat Biotechnol 27:760-U115. https://doi.org/10.1038/nbt.1555
Valle F, Munoz E, Ponce E, Flores N, Bolivar F (1996) Basic and applied aspects of metabolic diversity: the phosphoenolpyruvate node. J Ind Microbiol Biot 17:458–462. https://doi.org/10.1007/Bf01574776
Vernyik V et al (2020) Exploring the fitness benefits of genome reduction in Escherichia Coli by a selection-driven approach. Sci Rep 10(1):7345. https://doi.org/10.1038/s41598-020-64074-5
Viegas SC, Apura P, Martinez-Garcia E, de Lorenzo V, Arraiano CM (2018) Modulating heterologous gene expression with portable mRNA-stabilizing 5’-UTR sequences. ACS Synth Biol 7:2177–2188. https://doi.org/10.1021/acssynbio.8b00191
Vogel HJ (1957) Repressed and induced enzyme formation: a unified hypothesis. Proc Natl Acad Sci USA 43:491–496. https://doi.org/10.1073/pnas.43.6.491
Wang J, Cheng LK, Wang J, Liu Q, Shen T, Chen N (2013) Genetic engineering of Escherichia Coli to enhance production of L-Tryptophan. Appl Microbiol Biot 97:7587–7596. https://doi.org/10.1007/s00253-013-5026-3
Wang J, Shen XL, Rey J, Yuan QP, Yan YJ (2018) Recent advances in microbial production of aromatic natural products and their derivatives. Appl Microbiol Biot 102:47–61. https://doi.org/10.1007/s00253-017-8599-4
Watanabe T, Snell EE (1972) Reversibility of the tryptophanase reaction: synthesis of tryptophan from indole, pyruvate, and ammonia. Proc Natl Acad Sci USA 69:1086–1090. https://doi.org/10.1073/pnas.69.5.1086
Wei XX, Shi ZY, Li ZJ, Cai L, Wu Q, Chen GQ (2010) A Mini-Mu transposon-based method for multiple DNA fragment integration into bacterial genomes. Appl Microbiol Biot 87:1533–1541. https://doi.org/10.1007/s00253-010-2674-4
Weinert BT et al (2013) Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Mol Cell 51:265–272. https://doi.org/10.1016/j.molcel.2013.06.003
Whipp MJ, Pittard AJ (1995) A reassessment of the relationship between aroK-encoded and aroL-encoded shikimate kinase enzymes of Escherichia coli. J Bacteriol 177:1627–1629. https://doi.org/10.1128/jb.177.6.1627-1629.1995
Wolfe AJ (2005) The acetate switch microbiol. Mol Biol Rev 69(1):12–50. https://doi.org/10.1128/Mmbr.69.1.12-50.2005
Wolfe AJ (2010) Physiologically relevant small phosphodonors link metabolism to signal transduction. Curr Opin Microbiol 13:204–209. https://doi.org/10.1016/j.mib.2010.01.002
Xu QY, Bai F, Chen N, Bai G (2017) Gene modification of the acetate biosynthesis pathway in Escherichia Coli and implementation of the cell recycling technology to increase L-Tryptophan production. PLoS One 12(6):e0179240. https://doi.org/10.1371/journal.pone.0179240
Xu JZ, Yang HK, Zhang WG (2018) NADPH metabolism: a survey of its theoretical characteristics and manipulation strategies in amino acid biosynthesis. Crit Rev Biotechnol 38:1061–1076. https://doi.org/10.1080/07388551.2018.1437387
Xu Y et al (2020) An acid-tolerance response system protecting exponentially growing Escherichia Coli. Nat Commun 11(1):1496–1507. https://doi.org/10.1038/s41467-020-15350-5
Yakandawala N, Romeo T, Friesen AD, Madhyastha S (2008) Metabolic engineering of Escherichia Coli to enhance phenylalanine production. Appl Microbiol Biot 78:283–291. https://doi.org/10.1007/s00253-007-1307-z
Yang D, Yoo SM, Gu C, Ryu JY, Lee JE, Lee SY (2019) Expanded synthetic small regulatory RNA expression platforms for rapid and multiplex gene expression knockdown. Metab Eng 54:180–190. https://doi.org/10.1016/j.ymben.2019.04.003
Yang J, Chawla R, Rhee KY, Gupta R, Manson MD, Jayaraman A, Lele PP (2020) Biphasic chemotaxis of Escherichia Coli to the microbiota metabolite indole. Proc Natl Acad Sci USA 117:6114–6120. https://doi.org/10.1073/pnas.1916974117
Yanofsky C (2005) The favorable features of tryptophan synthase for proving Beadle and Tatum’s one gene-one enzyme hypothesis. Genetics 169:511–516
Yanofsky C, Horn V, Gollnick P (1991) Physiological studies of tryptophan transport and tryptophanase operon induction in Escherichia coli. J Bacteriol 173:6009–6017. https://doi.org/10.1128/jb.173.19.6009-6017.1991
Yu BJ et al (2002) Minimization of the Escherichia coli genome using a Tn5-targeted Cre/loxP excision system. Nat Biotechnol 20:1018–1023. https://doi.org/10.1038/nbt740
Yuan JJ, Zweers JC, van Dijl JM, Dalbey RE (2010) Protein transport across and into cell membranes in bacteria and archaea. Cell Mol Life Sci 67:179–199. https://doi.org/10.1007/s00018-009-0160-x
Zakataeva NP, Kutukova EA, Gronskiy SV, Troshin PV, Livshits VA, Aleshin VV (2006) Export of metabolites by the proteins of the DMT and RhtB families and its possible role in intercellular communication. Microbiology 75:438–448. https://doi.org/10.1134/S0026261706040126
Zeng WZ, Guo LK, Xu S, Chen J, Zhou JW (2020) High-throughput screening technology in industrial biotechnology. Trends Biotechnol 38:888–906. https://doi.org/10.1016/j.tibtech.2020.01.001
Zhang Y, Dong RN, Zhang MJ, Gao HJ (2018a) Native efflux pumps of Escherichia coli responsible for short and medium chain alcohol. Biochem Eng J 133:149–156. https://doi.org/10.1016/j.bej.2018.02.009
Zhang Y et al (2018b) Reprogramming one carbon metabolic pathways to decouple L-Serine catabolism from cell growth in Corynebacterium Glutamicum. ACS Synth Biol 7:635–646. https://doi.org/10.1021/acssynbio.7b00373
Zhang XM et al (2019) High-Yield Production of L-Serine from Glycerol by Engineered Escherichia Coli. J Ind Microbiol Biot 46:883–885. https://doi.org/10.1007/s10295-019-02163-9
Zhao ZJ et al (2011) Development of L-Tryptophan production strains by defined genetic modification in Escherichia Coli. J Ind Microbiol Biot 38:1921–1929. https://doi.org/10.1007/s10295-011-0978-8
Zhao ZJ, Chen S, Wu D, Wu J, Chen J (2012) Effect of gene knockouts of L-tryptophan uptake system on the production of L-tryptophan in Escherichia coli. Process Biochem 47:340–344. https://doi.org/10.1016/j.procbio.2011.11.009
Zhao GJ, Hu TY, Li J, Wei H, Shang H, Guan YF (2015) A novel strategy to analyze L-tryptophan through allosteric Trp repressor based on rolling circle amplification. Biosens Bioelectron 71:103–107. https://doi.org/10.1016/j.bios.2015.04.017
Zhao CG, Cheng LK, Wang J, Shen ZQ, Chen N (2016a) Impact of deletion of the genes encoding acetate kinase on production of L-tryptophan by Escherichia coli. Ann Microbiol 66:261–269. https://doi.org/10.1007/s13213-015-1103-4
Zhao Y, Wang CS, Li FF, Liu ZN, Zhao GR (2016b) Targeted optimization of central carbon metabolism for engineering succinate production in Escherichia coli. BMC Biotechnol 16:52. https://doi.org/10.1186/s12896-016-0284-7
Zhu J, Song SQ, Sun ZH, Lian LD, Shi L, Ren A, Zhao MW (2021) Regulation of glutamine synthetase activity by transcriptional and posttranslational modifications negatively influences ganoderic acid biosynthesis in Ganoderma lucidum. Environ Microbiol 23:1286–1297. https://doi.org/10.1111/1462-2920.15400
Acknowledgements
We thank Prof. Zhi-Ming Rao from School of Biotechnology at Jiangnan University for assistance in manuscript writing. This work was financially supported by the National Key Research and Development Program of China (2021YFC2100900), the Key Laboratory of Industrial Biotechnology, Ministry of Education, Jiangnan University (KLIB-KF 202004), and Fundamental Research Funds for the Central Universities [No. JUSRP115A19].
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Liu, S., Xu, JZ. & Zhang, WG. Advances and prospects in metabolic engineering of Escherichia coli for L-tryptophan production. World J Microbiol Biotechnol 38, 22 (2022). https://doi.org/10.1007/s11274-021-03212-1
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DOI: https://doi.org/10.1007/s11274-021-03212-1