Shikimic acid production in Escherichia coli: From classical metabolic engineering strategies to omics applied to improve its production

Frontiers in Bioengineering and Biotechnology

Volumn 3, Issue SEP, 2015, Pages

  Martínez, Juan Andrés ^a   Bolívar, Francisco ^a   Escalante, Adelfo ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Antiviral drug; Escherichia coli; Influenza; Metabolic engineering; Metabolome; Shikimic acid; Transcriptome

Indexed keywords

BACTERIA; BATCH CELL CULTURE; BIOCONVERSION; CARBOXYLIC ACIDS; ESCHERICHIA COLI; GENES; INDUSTRIAL PLANTS; METABOLISM; PLANNING; STRAIN; VIRUSES;

ANTI-VIRAL DRUGS; INFLUENZA; METABOLOMES; SHIKIMIC ACIDS; TRANSCRIPTOMES;

METABOLIC ENGINEERING;

EID: 85011654981     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2015.00145     Document Type: Review

References (68)

1. Aguilar, C., Escalante, A., Flores, N., de Anda, R., Riveros-McKay, F., Gosset, G., et al. (2012). Genetic changes during a laboratory adaptive evolution process that allowed fast growth in glucose to an Escherichia coli strain lacking the major glucose transport system. BMC Genomics 13:385. doi:10.1186/1471-2164-13-385
2. Åkesson, M., Förster, J., and Nielsen, J. (2004). Integration of gene expression data into genome-scale metabolic models. Metab. Eng. 6, 285-293. doi:10.1016/j.ymben.2003.12.002
3. Báez, J. L., Bolívar, F., and Gosset, G. (2001). Determination of 3-deoxy-D-arabino-heptulosonate 7-phosphate productivity and yield from glucose in Escherichia coli devoid of the glucose phosphotransferase transport system. Biotechnol. Bioeng. 73, 530-535. doi:10.1002/bit.1088
4. Báez-Viveros, J. L., Osuna, J., Hernández-Chávez, G., Soberón, X., Bolívar, F., and Gosset, G. (2004). Metabolic engineering and protein directed evolution increase the yield of L-phenylalanine synthesized from glucose in Escherichia coli. Biotechnol. Bioeng. 87, 516-524. doi:10.1002/bit.20159
5. Biggs, B. W., De Paepe, B., Santos, C. N. S., De Mey, M., and Kumaran Ajikumar, P. (2014). Multivariate modular metabolic engineering for pathway and strain optimization. Curr. Opin. Biotechnol. 29, 156-162. doi:10.1016/j.copbio.2014.05.005
6. Bongaerts, J. (2001). Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab. Eng. 3, 289-300. doi:10.1006/mben.2001.0196
7. Chandran, S. S., Yi, J., Draths, K. M., von Daeniken, R., Weber, W., and Frost, J. W. (2003). Phosphoenolpyruvate availability and the biosynthesis of shikimic acid. Biotechnol. Prog. 19, 808-814. doi:10.1021/bp025769p
8. Chen, K., Dou, J., Tang, S., Yang, Y., Wang, H., Fang, H., et al. (2012). Deletion of the aroK gene is essential for high shikimic acid accumulation through the shikimate pathway in E. coli. Bioresour. Technol. 119, 141-147. doi:10.1016/j.biortech.2012.05.100
9. Chen, P. T., Chiang, C.-J., Wang, J.-Y., Lee, M.-Z., and Chao, Y.-P. (2011). Genomic engineering of Escherichia coli for production of intermediate metabolites in the aromatic pathway. J. Taiwan Inst. Chem. Eng. 42, 34-40. doi:10.1016/j.jtice.2010.03.010
10. Chen, X., Li, M., Zhou, L., Shen, W., Algasan, G., Fan, Y., et al. (2014). Metabolic engineering of Escherichia coli for improving shikimate synthesis from glucose. Bioresour. Technol. 166, 64-71. doi:10.1016/j.biortech.2014.05.035
11. Chen, X., Zhou, L., Tian, K., Kumar, A., Singh, S., Prior, B. A., et al. (2013). Metabolic engineering of Escherichia coli: a sustainable industrial platform for bio-based chemical production. Biotechnol. Adv. 31, 1200-1223. doi:10.1016/j.biotechadv.2013.02.009
12. Cloots, L., and Marchal, K. (2011). Network-based functional modeling of genomics, transcriptomics and metabolism in bacteria. Curr. Opin. Microbiol. 14, 599-607. doi:10.1016/j.mib.2011.09.003
13. Cortés-Tolalpa, L., Gutiérrez-Ríos, R. M., Martínez, L. M., De Anda, R., Gosset, G., Bolívar, F., et al. (2014). Global transcriptomic analysis of an engineered Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system during shikimic acid production in rich culture medium. Microb. Cell Fact. 13, 28. doi:10.1186/1475-2859-13-28
14. Covert, M. W., Schilling, C. H., Famili, I., Edwards, J. S., Goryanin, I. I., Selkov, E., et al. (2001). Metabolic modeling of microbial strains in silico. Trends Biochem. Sci. 26, 179-186. doi:10.1016/S0968-0004(00)01754-0
15. Cui, Y.-Y., Ling, C., Zhang, Y.-Y., Huang, J., and Liu, J.-Z. (2014). Production of shikimic acid from Escherichia coli through chemically inducible chromosomal evolution and cofactor metabolic engineering. Microb. Cell Fact. 13, 21. doi:10.1186/1475-2859-13-21
16. Díaz Quiroz, D. C., Carmona, S. B., Bolívar, F., and Escalante, A. (2014). Current perspectives on applications of shikimic acid aminoshikimic acids in pharmaceutical chemistry. Res. Rep. Med. Chem. 4, 35-46. doi:10.2147/RRMC.S46560
17. Draths, K. M., Knop, D. R., and Frost, J. W. (1999). Shikimic acid and quinic acid: replacing isolation from plant sources with recombinant microbial biocatalysis. J. Am. Chem. Soc. 121, 1603-1604. doi:10.1021/ja9830243
18. Escalante, A., Calderón, R., Valdivia, A., de Anda, R., Hernández, G., Ramírez, O. T., et al. (2010). Metabolic engineering for the production of shikimic acid in an evolved Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Microb. Cell Fact. 9, 21. doi:10.1186/1475-2859-9-21
19. Escalante, A., Salinas Cervantes, A., Gosset, G., and Bolívar, F. (2012). Current knowledge of the Escherichia coli phosphoenolpyruvate-carbohydrate phosphotransferase system: peculiarities of regulation and impact on growth and product formation. Appl. Microbiol. Biotechnol. 94, 1483-1494. doi:10.1007/s00253-012-4101-5
20. Estevez, A., and Estevez, R. (2012). A short overview on the medicinal chemistry of (-)-shikimic acid. Mini Rev. Med. Chem. 12, 1443-1454. doi:10.2174/138955712803832735
21. F. Hoffmann-La Roche Ltd. (2009). Roche Annual Report 09. Basel, Switzerland: F. Hoffmnn-La Roche Ltd. 127 p. Available at: http://www.roche.com/gb09e.pdf
22. Flores, N., Leal, L., Sigala, J. C., de Anda, R., Escalante, A., Martínez, A., et al. (2007). Growth recovery on glucose under aerobic conditions of an Escherichia coli strain carrying a phosphoenolpyruvate: carbohydrate phosphotransferase system deletion by inactivating arcA and overexpressing the genes coding for glucokinase and galactose permease. J. Mol. Microbiol. Biotechnol. 13, 105-116. doi:10.1159/000103602
23. Flores, N., Xiao, J., Berry, A., Bolivar, F., and Valle, F. (1996). Pathway engineering for the production of aromatic compounds in Escherichia coli. Nat. Biotechnol. 14, 620-623. doi:10.1038/nbt0596-620
24. Fong, S. S. (2014). Computational approaches to metabolic engineering utilizing systems biology and synthetic biology. Comput. Struct. Biotechnol. J. 11, 28-34. doi:10.1016/j.csbj.2014.08.005
25. Frost, J. W., Frost, K. M., and Knop, D. R. (2002). Biocatalytic Synthesis of Shikimic Acid. Available at: http://www.google.com/patents/US6472169 (accessed July 5, 2015).
26. Ghosh, S., Chisti, Y., and Banerjee, U. C. (2012). Production of shikimic acid. Biotechnol. Adv. 30, 1425-1431. doi:10.1016/j.biotechadv.2012.03.001
27. Gosset, G. (2009). Production of aromatic compounds in bacteria. Curr. Opin. Biotechnol. 20, 651-658. doi:10.1016/j.copbio.2009.09.012
28. Johansson, L., and Lidén, G. (2006). Transcriptome analysis of a shikimic acid producing strain of Escherichia coli W3110 grown under carbon-and phosphate-limited conditions. J. Biotechnol. 126, 528-545. doi:10.1016/j.jbiotec.2006.05.007
29. Johansson, L., Lindskog, A., Silfversparre, G., Cimander, C., Nielsen, K. F., and Lidén, G. (2005). Shikimic acid production by a modified strain of E. coli (W3110.shik1) under phosphate-limited and carbon-limited conditions. Biotechnol. Bioeng. 92, 541-552. doi:10.1002/bit.20546
30. Jouhten, P. (2012). Metabolic modelling in the development of cell factories by synthetic biology. Comput. Struct. Biotechnol. J. 3, 1-9. doi:10.5936/csbj.201210009
31. Juminaga, D., Baidoo, E. E. K., Redding-Johanson, A. M., Batth, T. S., Burd, H., Mukhopadhyay, A., et al. (2012). Modular engineering of L-tyrosine production in Escherichia coli. Appl. Environ. Microbiol. 78, 89-98. doi:10.1128/AEM.06017-11
32. Kedar, P., Colah, R., and Shimizu, K. (2007). Proteomic investigation on the pyk-F gene knockout Escherichia coli for aromatic amino acid production. Enzyme Micro. Technol. 41, 455-465. doi:10.1016/j.enzmictec.2007.03.018
33. Kern, R., Malki, A., Abdallah, J., Tagourti, J., and Richarme, G. (2006). Escherichia coli HdeB is an acid stress chaperone. J. Bacteriol. 189, 603-610. doi:10.1128/JB.01522-06
34. Keseler, I. M., Mackie, A., Peralta-Gil, M., Santos-Zavaleta, A., Gama-Castro, S., Bonavides-Martínez, C., et al. (2013). EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41, D605-D612. doi:10.1093/nar/gks1027
35. Khodayari, A., Zomorrodi, A. R., Liao, J. C., and Maranas, C. D. (2014). A kinetic model of Escherichia coli core metabolism satisfying multiple sets of mutant flux data. Metab. Eng. 25, 50-62. doi:10.1016/j.ymben.2014.05.014
36. Kim, T. Y., Sohn, S. B., Kim, Y. B., Kim, W. J., and Lee, S. Y. (2012). Recent advances in reconstruction and applications of genome-scale metabolic models. Curr. Opin. Biotechnol. 23, 617-623. doi:10.1016/j.copbio.2011.10.007
37. King, Z. A., Lloyd, C. J., Feist, A. M., and Palsson, B. O. (2015). Next-generation genome-scale models for metabolic engineering. Curr. Opin. Biotechnol. 35, 23-29. doi:10.1016/j.copbio.2014.12.016
38. Knop, D. R., Draths, K. M., Chandran, S. S., Barker, J. L., von Daeniken, R., Weber, W., et al. (2001). Hydroaromatic equilibration during biosynthesis of shikimic acid. J. Am. Chem. Soc. 123, 10173-10182. doi:10.1021/ja0109444
39. Krämer, M., Bongaerts, J., Bovenberg, R., Kremer, S., Müller, U., Orf, S., et al. (2003). Metabolic engineering for microbial production of shikimic acid. Metab. Eng. 5, 277-283. doi:10.1016/j.ymben.2003.09.001
40. Krull, R., and Wittmann, C. (2010). Linking Cellular Networks and Bioprocesses. Heidelberg: Springer.
41. Li, S., Yuan, W., Wang, P., Zhang, Z., Zhang, W., and Ownby, S. (2007). Method for the Extraction and Purification of Shikimic Acid. Available at: http://www.google.com/patents/US20070149805
42. Lin, S., Liang, R., Meng, X., OuYang, H., Yan, H., Wang, Y., et al. (2014). Construction and expression of mutagenesis strain of aroG gene from Escherichia coli K-12. Int. J. Biol. Macromol. 68, 173-177. doi:10.1016/j.ijbiomac.2014.04.034
43. Liu, A., Liu, Z. Z., Zou, Z. M., Chen, S. Z., Xu, L. Z., and Yang, S. L. (2004). Synthesis of (+)-zeylenone from shikimic acid. Tetrahedron 60, 3689-3694. doi:10.1016/j.tet.2004.02.066
44. Liu, Q., Cheng, Y., Xie, X., Xu, Q., and Chen, N. (2012). Modification of tryptophan transport system and its impact on production of L-tryptophan in Escherichia coli. Bioresour. Technol. 114, 549-554. doi:10.1016/j.biortech.2012.02.088
45. Long, M. R., Ong, W. K., and Reed, J. L. (2015). Computational methods in metabolic engineering for strain design. Curr. Opin. Biotechnol. 34, 135-141. doi:10.1016/j.copbio.2014.12.019
46. Lütke-Eversloh, T., and Stephanopoulos, G. (2008). Combinatorial pathway analysis for improved L-tyrosine production in Escherichia coli: identification of enzymatic bottlenecks by systematic gene overexpression. Metab. Eng. 10, 69-77. doi:10.1016/j.ymben.2007.12.001
47. Machado, D., and Herrgård, M. (2014). Systematic evaluation of methods for integration of transcriptomic data into constraint-based models of metabolism. PLoS Comput. Biol. 10:e1003580. doi:10.1371/journal.pcbi.1003580
48. Matsuoka, Y., and Shimizu, K. (2012). Importance of understanding the main metabolic regulation in response to the specific pathway mutation for metabolic engineering of Escherichia coli. Comput. Struct. Biotechnol. J. 3, 1-10. doi:10.5936/csbj.201210018
49. O'Brien, E. J., and Palsson, B. O. (2015). Computing the functional proteome: recent progress and future prospects for genome-scale models. Curr. Opin. Biotechnol. 34, 125-134. doi:10.1016/j.copbio.2014.12.017
50. Patil, K. R., Åkesson, M., and Nielsen, J. (2004). Use of genome-scale microbial models for metabolic engineering. Curr. Opin. Biotechnol. 15, 64-69. doi:10.1016/j.copbio.2003.11.003
51. Patnaik, R., and Liao, J. C. (1994). Engineering of Escherichia coli central metabolism for aromatic metabolite production with near theoretical yield. Appl. Environ. Microbiol. 60, 3903-3908.
52. Patnaik, R., Spitzer, R. G., and Liao, J. C. (1995). Pathway engineering for production of aromatics in Escherichia coli: confirmation of stoichiometric analysis by independent modulation of AroG, TktA, and Pps activities. Biotechnol. Bioeng. 46, 361-370. doi:10.1002/bit.260460409
53. Pharkya, P., Burgard, A. P., and Maranas, C. D. (2003). Exploring the overproduction of amino acids using the bilevel optimization framework OptKnock. Biotechnol. Bioeng. 84, 887-899. doi:10.1002/bit.10857
54. Price, N. D., Papin, J. A., Schilling, C. H., and Palsson, B. O. (2003). Genome-scale microbial in silico models: the constraints-based approach. Trends Biotechnol. 21, 162-169. doi:10.1016/S0167-7799(03)00030-1
55. Raghavendra, T. R., Vaidyanathan, P., Swathi, H. K., Ramesha, B. T., Ravikanth, G., Ganeshaiah, K. N., et al. (2009). Prospecting for alternate sources of shikimic acid, a precursor of Tamiflu, a bird-flu drug. Curr. Sci. 96, 771-772.
56. Rangachari, S., Friedamna, T. C., Hartmann, R., and Weisenfeld, R. B. (2013). Processes for Producing and Recovering Shikimic Acid. Available at: http://www.google.com/patents/US8344178 (accessed July 5, 2015).
57. Rizk, M. L., and Liao, J. C. (2009). Ensemble modeling for aromatic production in Escherichia coli. PLoS ONE 4:e6903. doi:10.1371/journal.pone.0006903
58. Rodriguez, A., Martínez, J. A., Báez-Viveros, J. L., Flores, N., Hernández-Chávez, G., Ramírez, O. T., et al. (2013). Constitutive expression of selected genes from the pentose phosphate and aromatic pathways increases the shikimic acid yield in high-glucose batch cultures of an Escherichia coli strain lacking PTS and pykF. Microb. Cell Fact. 12, 86. doi:10.1186/1475-2859-12-86
59. Rodriguez, A., Martinez, J. A., Flores, N., Escalante, A., Gosset, G., and Bolivar, F. (2014). Engineering Escherichia coli to overproduce aromatic amino acids and derived compounds. Microb. Cell Fact. 13, 126. doi:10.1186/s12934-014-0126-z
60. Saha, R., Chowdhury, A., and Maranas, C. D. (2014). Recent advances in the reconstruction of metabolic models and integration of omics data. Curr. Opin. Biotechnol. 29, 39-45. doi:10.1016/j.copbio.2014.02.011
61. Scheiwiller, T., and Hirschi, S. (2010). 09 Roche Annual Report. Finance Report. Basel: F. Horrmann-LaRoche Ltd.
62. Schuetz, R., Kuepfer, L., and Sauer, U. (2007). Systematic evaluation of objective functions for predicting intracellular fluxes in Escherichia coli. Mol. Syst. Biol. 3, 119. doi:10.1038/msb4100162
63. Stelling, J. (2004). Mathematical models in microbial systems biology. Curr. Opin. Microbiol. 7, 513-518. doi:10.1016/j.mib.2004.08.004
64. Wang, G.-W., Hu, W.-T., Huang, B.-K., and Qin, L.-P. (2011). Illicium verum: a review on its botany, traditional use, chemistry and pharmacology. J. Ethnopharmacol. 136, 10-20. doi:10.1016/j.jep.2011.04.051
65. World Health Organization. (2011). Pandemic Influenza Preparedness. Framework for the Sharing of Influenza Viruses and Access to Vaccines and Other Benefits. France: World Health Organization. Available at: http://www.who.int/influenza/resources/pip_framework/en/
66. Yi, J., Li, K., Draths, K. M., and Frost, J. W. (2002). Modulation of phosphoenolpyruvate synthase expression increases shikimate pathway product yields in E. coli. Biotechnol. Prog. 18, 1141-1148. doi:10.1021/bp020101w
67. Zhang, B., Zhou, N., Liu, Y.-M., Liu, C., Lou, C.-B., Jiang, C.-Y., et al. (2015). Ribosome binding site libraries and pathway modules for shikimic acid synthesis with Corynebacterium glutamicum. Microb. Cell Fact. 14, 71. doi:10.1186/s12934-015-0254-0
68. Zucko, J., Dunlap, W. C., Shick, J. M., Cullum, J., Cercelet, F., Amin, B., et al. (2010). Global genome analysis of the shikimic acid pathway reveals greater gene loss in host-associated than in free-living bacteria. BMC Genomics 11:628. doi:10.1186/1471-2164-11-628