Synthetic Pathway for the Production of Olivetolic Acid in Escherichia coli

ACS Synthetic Biology

Volumn 7, Issue 8, 2018, Pages 1886-1896

  Tan, Zaigao ^a   Clomburg, James M ^a   Gonzalez, Ramon ^a  

^a Rice University   (United States)

Author keywords

natural products; olivetolic acid (OLA); synthetic biology; type III polyketide synthases (PKS III)

Indexed keywords

BACTERIAL ENZYME; MALONYL COENZYME A; OLIVETOLIC ACID; POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG; SALICYLIC ACID DERIVATIVE;

ARTICLE; BIOSYNTHESIS; CARBON SOURCE; CATALYSIS; ENZYME SYNTHESIS; ESCHERICHIA COLI; FATTY ACID OXIDATION; FERMENTATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PRENYLATION; ENZYMOLOGY; METABOLISM; SYNTHETIC BIOLOGY;

ESCHERICHIA COLI; POLYKETIDE SYNTHASES; SALICYLATES; SYNTHETIC BIOLOGY;

EID: 85049681840     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.8b00075     Document Type: Article

References (50)

1. Zhou, W., Zhuang, Y., Bai, Y., Bi, H., Liu, T., and Ma, Y. (2016) Biosynthesis of phlorisovalerophenone and 4-hydroxy-6-isobutyl-2-pyrone in Escherichia coli from glucose. Microb. Cell Fact. 15, 149, 10.1186/s12934-016-0549-9
2. Yu, D. Y., Xu, F. C., Zeng, J., and Zhan, J. X. (2012) Type III polyketide synthases in natural product biosynthesis. IUBMB Life 64, 285-295, 10.1002/iub.1005
3. Li, H., Liang, J., Chen, H., Ding, G., Ma, B., and He, N. (2016) Evolutionary and functional analysis of mulberry type III polyketide synthases. BMC Genomics 17, 540, 10.1186/s12864-016-2843-7
4. Ismed, F., Farhan, A., Bakhtiar, A., Zaini, F., Nugraha, Y. P., Putra, O. D., and Uckusa, H. (2016) Crystal structure of olivetolic acid: a natural product from Cetrelia sanguinea (Schaer. Acta Crystallogr. E 72, 1587-1589, 10.1107/S2056989016016273
5. Costain, W. J., Tauskela, J. S., Rasquinha, I., Comas, T., Hewitt, M., Marleau, V., and Soo, E. C. (2016) Pharmacological characterization of emerging synthetic cannabinoids in HEK293T cells and hippocampal neurons. Eur. J. Pharmacol. 786, 234-245, 10.1016/j.ejphar.2016.05.040
6. Tai, S. and Fantegrossi, W. E. (2014) Synthetic Cannabinoids: Pharmacology, Behavioral Effects, and Abuse Potential. Current addiction reports. 1, 129-136, 10.1007/s40429-014-0014-y
7. Huestis, M. A. (2007) Human cannabinoid pharmacokinetics. Chem. Biodiversity 4, 1770-1804, 10.1002/cbdv.200790152
8. Andre, C. M., Hausman, J. F., and Guerriero, G. (2016) Cannabis sativa: The Plant of the Thousand and One Molecules. Front. Plant Sci. 10.3389/fpls.2016.00019
9. Hazekamp, A., Simons, R., Peltenburg-Looman, A., Sengers, M., van Zweden, R., and Verpoorte, R. (2004) Preparative isolation of cannabinoids from Cannabis sativa by centrifugal partition chromatography. J. Liq. Chromatogr. Relat. Technol. 27, 2421-2439, 10.1081/JLC-200028170
10. Yoshimatsu, K., Iida, O., Kitazawa, T., Sekine, T., Kojoma, M., Makino, Y., and Kiuchi, F. (2004) Growth characteristics of Cannabis sativa L. cultivated in a phytotron and in the field. Kokuritsu Iyakuhin Shokuhin Eisei Kenkyujo Hokoku 16-20
11. Yao, J., Weng, Y. Q., Dickey, A., and Wang, K. Y. (2015) Plants as Factories for Human Pharmaceuticals: Applications and Challenges. Int. J. Mol. Sci. 16, 28549-28565, 10.3390/ijms161226122
12. Chittiboyina, A. and Khan, I. (2012) Short synthesis of olivetolic acid via Directed ortho-Metalation (DoM). Planta Med. 78, 42, 10.1055/s-0032-1307550
13. Liu, X., Ding, W., and Jiang, H. (2017) Engineering microbial cell factories for the production of plant natural products: from design principles to industrial-scale production. Microb. Cell Fact. 16, 125, 10.1186/s12934-017-0732-7
14. Ajikumar, P. K., Xiao, W. H., Tyo, K. E., Wang, Y., Simeon, F., Leonard, E., Mucha, O., Phon, T. H., Pfeifer, B., and Stephanopoulos, G. (2010) Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli. Science 330, 70-74, 10.1126/science.1191652
15. Bai, Y., Yin, H., Bi, H., Zhuang, Y., Liu, T., and Ma, Y. (2016) De novo biosynthesis of Gastrodin in Escherichia coli. Metab. Eng. 35, 138-147, 10.1016/j.ymben.2016.01.002
16. Ro, D. K., Paradise, E. M., Ouellet, M., Fisher, K. J., Newman, K. L., Ndungu, J. M., Ho, K. A., Eachus, R. A., Ham, T. S., Kirby, J., Chang, M. C., Withers, S. T., Shiba, Y., Sarpong, R., and Keasling, J. D. (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440, 940-943, 10.1038/nature04640
17. Taura, F., Tanaka, S., Taguchi, C., Fukamizu, T., Tanaka, H., Shoyama, Y., and Morimoto, S. (2009) Characterization of olivetol synthase, a polyketide synthase putatively involved in cannabinoid biosynthetic pathway. FEBS Lett. 583, 2061-2066, 10.1016/j.febslet.2009.05.024
18. Gagne, S. J., Stout, J. M., Liu, E., Boubakir, Z., Clark, S. M., and Page, J. E. (2012) Identification of olivetolic acid cyclase from Cannabis sativa reveals a unique catalytic route to plant polyketides. Proc. Natl. Acad. Sci. U. S. A. 109, 12811-12816, 10.1073/pnas.1200330109
19. Krivoruchko, A., Zhang, Y., Siewers, V., Chen, Y., and Nielsen, J. (2015) Microbial acetyl-CoA metabolism and metabolic engineering. Metab. Eng. 28, 28-42, 10.1016/j.ymben.2014.11.009
20. Vadali, R. V., Horton, C. E., Rudolph, F. B., Bennett, G. N., and San, K. Y. (2004) Production of isoamyl acetate in ackA-pta and/or ldh mutants of Escherichia coli with overexpression of yeast ATF2. Appl. Microbiol. Biotechnol. 63, 698-704, 10.1007/s00253-003-1452-y
21. Lin, F., Chen, Y., Levine, R., Lee, K., Yuan, Y., and Lin, X. N. (2013) Improving fatty acid availability for bio-hydrocarbon production in Escherichia coli by metabolic engineering. PLoS One 8, e78595, 10.1371/journal.pone.0078595
22. Zhou, S., Iverson, A. G., and Grayburn, W. S. (2008) Engineering a native homoethanol pathway in Escherichia coli B for ethanol production. Biotechnol. Lett. 30, 335-342, 10.1007/s10529-007-9544-x
23. Dellomonaco, C., Clomburg, J. M., Miller, E. N., and Gonzalez, R. (2011) Engineered reversal of the beta-oxidation cycle for the synthesis of fuels and chemicals. Nature 476, 355-359, 10.1038/nature10333
24. Kim, S., Clomburg, J. M., and Gonzalez, R. (2015) Synthesis of medium-chain length (C6-C10) fuels and chemicals via beta-oxidation reversal in Escherichia coli. J. Ind. Microbiol. Biotechnol. 42, 465-475, 10.1007/s10295-015-1589-6
25. Yang, J., Xiong, Z. Q., Song, S. J., Wang, J. F., Lv, H. J., and Wang, Y. (2015) Improving heterologous polyketide production in Escherichia coli by transporter engineering. Appl. Microbiol. Biotechnol. 99, 8691-8700, 10.1007/s00253-015-6718-7
26. Kim, Y. S. and Bang, S. K. (1985) Malonyl coenzyme A synthetase. Purification and properties. J. Biol. Chem. 260, 5098-5104
27. Kim, Y. S. and Kang, S. W. (1994) Steady-state kinetics of malonyl-CoA synthetase from Bradyrhizobium japonicum and evidence for Malonyl-AMP formation in the reaction. Biochem. J. 297, 327-333, 10.1042/bj2970327
28. Wolfe, A. J. (2005) The acetate switch. Microbiology and molecular biology reviews: MMBR. 69, 12-50, 10.1128/MMBR.69.1.12-50.2005
29. Davis, M. S., Solbiati, J., and Cronan, J. E., Jr (2000) Overproduction of acetyl-CoA carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J. Biol. Chem. 275, 28593-28598, 10.1074/jbc.M004756200
30. Shi, S. B., Chen, Y., Siewers, V., and Nielsen, J. (2014) Improving production of malonyl coenzyme A-derived metabolites by abolishing Snf1-dependent regulation of Acc1. mBio 5, e01130-14, 10.1128/mBio.01130-14
31. Campbell, J. W., Morgan-Kiss, R. M., and Cronan, J. E. (2003) A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic beta-oxidation pathway. Mol. Microbiol. 47, 793-805, 10.1046/j.1365-2958.2003.03341.x
32. Morgan-Kiss, R. M. and Cronan, J. E. (2004) The Escherichia coli fadK (ydiD) gene encodes an anerobically regulated short chain acyl-CoA synthetase. J. Biol. Chem. 279, 37324-37333, 10.1074/jbc.M405233200
33. Dirusso, C. C. and Black, P. N. (2004) Bacterial long chain fatty acid transport: gateway to a fatty acid-responsive signaling system. J. Biol. Chem. 279, 49563-49566, 10.1074/jbc.R400026200
34. Ford, T. J. and Way, J. C. (2015) Enhancement of E. Coli acyl-CoA synthetase FadD activity on medium chain fatty acids. PeerJ. 3, e1040, 10.7717/peerj.1040
35. Jarboe, L. R., Zhang, X., Wang, X., Moore, J. C., Shanmugam, K. T., and Ingram, L. O. (2010) Metabolic engineering for production of biorenewable fuels and chemicals: contributions of synthetic biology. J. Biomed. Biotechnol. 2010, 761042, 10.1155/2010/761042
36. Monk, J. M., Charusanti, P., Aziz, R. K., Lerman, J. A., Premyodhin, N., Orth, J. D., Feist, A. M., and Palsson, B. O. (2013) Genome-scale metabolic reconstructions of multiple Escherichia coli strains highlight strain-specific adaptations to nutritional environments. Proc. Natl. Acad. Sci. U. S. A. 110, 20338-20343, 10.1073/pnas.1307797110
37. Clomburg, J. M., Blankschien, M. D., Vick, J. E., Chou, A., Kim, S., and Gonzalez, R. (2015) Integrated engineering of beta-oxidation reversal and omega-oxidation pathways for the synthesis of medium chain omega-functionalized carboxylic acids. Metab. Eng. 28, 202-212, 10.1016/j.ymben.2015.01.007
38. Torella, J. P., Ford, T. J., Kim, S. N., Chen, A. M., Way, J. C., and Silver, P. A. (2013) Tailored fatty acid synthesis via dynamic control of fatty acid elongation. Proc. Natl. Acad. Sci. U. S. A. 110, 11290-11295, 10.1073/pnas.1307129110
39. Jing, F. Y., Cantu, D. C., Tvaruzkova, J., Chipman, J. P., Nikolau, B. J., Yandeau-Nelson, M. D., and Reilly, P. J. (2011) Phylogenetic and experimental characterization of an acyl-ACP thioesterase family reveals significant diversity in enzymatic specificity and activity. BMC Biochem. 12, 44, 10.1186/1471-2091-12-44
40. Tee, T. W., Chowdhury, A., Maranas, C. D., and Shanks, J. V. (2014) Systems metabolic engineering design: fatty acid production as an emerging case study. Biotechnol. Bioeng. 111, 849-857, 10.1002/bit.25205
41. Funa, N., Ohnishi, Y., Ebizuka, Y., and Horinouchi, S. (2002) Properties and substrate specificity of RppA, a chalcone synthase-related polyketide synthase in Streptomyces griseus. J. Biol. Chem. 277, 4628-4635, 10.1074/jbc.M110357200
42. Cheong, S., Clomburg, J. M., and Gonzalez, R. (2016) Energy- and carbon-efficient synthesis of functionalized small molecules in bacteria using non-decarboxylative Claisen condensation reactions. Nat. Biotechnol. 34, 556-561, 10.1038/nbt.3505
43. Baneyx, F. (1999) Recombinant protein expression in Escherichia coli. Curr. Opin. Biotechnol. 10, 411-421, 10.1016/S0958-1669(99)00003-8
44. Sriubolmas, N., Panbangred, W., Sriurairatana, S., and Meevootisom, V. (1997) Localization and characterization of inclusion bodies in recombinant Escherichia coli cells overproducing penicillin G acylase. Appl. Microbiol. Biotechnol. 47, 373-378, 10.1007/s002530050943
45. Mullick, A., Xu, Y., Warren, R., Koutroumanis, M., Guilbault, C., Broussau, S., Malenfant, F., Bourget, L., Lamoureux, L., Lo, R., Caron, A. W., Pilotte, A., and Massie, B. (2006) The cumate gene-switch: a system for regulated expression in mammalian cells. BMC Biotechnol. 6, 43, 10.1186/1472-6750-6-43
46. Schink, B., Philipp, B., and Muller, J. (2000) Anaerobic degradation of phenolic compounds. Naturwissenschaften 87, 12-23, 10.1007/s001140050002
47. Neidhardt, F. C., Bloch, P. L., and Smith, D. F. (1974) Culture medium for enterobacteria. J. Bacteriol. 119, 736-747
48. Bai, Y., Bi, H., Zhuang, Y., Liu, C., Cai, T., Liu, X., Zhang, X., Liu, T., and Ma, Y. (2015) Production of salidroside in metabolically engineered Escherichia coli. Sci. Rep. 4, 6640, 10.1038/srep06640
49. Bi, H., Bai, Y., Cai, T., Zhuang, Y., Liang, X., Zhang, X., Liu, T., and Ma, Y. (2013) Engineered short branched-chain acyl-CoA synthesis in E. Coli and acylation of chloramphenicol to branched-chain derivatives. Appl. Microbiol. Biotechnol. 97, 10339-10348, 10.1007/s00253-013-5262-6
50. Clomburg, J. M., Vick, J. E., Blankschien, M. D., Rodriguez-Moya, M., and Gonzalez, R. (2012) A synthetic biology approach to engineer a functional reversal of the beta-oxidation cycle. ACS Synth. Biol. 1, 541-554, 10.1021/sb3000782