Development of a Synthetic Malonyl-CoA Sensor in Saccharomyces cerevisiae for Intracellular Metabolite Monitoring and Genetic Screening

ACS Synthetic Biology

Volumn 4, Issue 12, 2015, Pages 1308-1315

  Li, Sijin ^a   Si, Tong ^a   Wang, Meng ^a   Zhao, Huimin ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

3 hydroxypropionic acid; genetic sensor; genome wide library; high throughput screening; malonyl CoA

Indexed keywords

HYDRACRYLIC ACID; MALONYL COENZYME A; TRANSCRIPTION FACTOR; ESCHERICHIA COLI PROTEIN; FAPR PROTEIN, E COLI;

ARTICLE; BACTERIAL GENETICS; CONTROLLED STUDY; ENZYMIC BIOSENSOR; FUNGAL STRAIN; GENE LIBRARY; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC SCREENING; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST; BIOSYNTHESIS; GENETIC PROCEDURES; GENETICS; METABOLISM; OPERATOR GENE; PROCEDURES;

BIOSENSING TECHNIQUES; ESCHERICHIA COLI PROTEINS; MALONYL COENZYME A; OPERATOR REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS;

EID: 84945270373     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.5b00069     Document Type: Article

References (57)

1. Keasling, J. D. (2010) Manufacturing molecules through metabolic engineering Science 330, 1355-1358 10.1126/science.1193990
2. Kim, B., Du, J., Eriksen, D. T., and Zhao, H. (2013) Combinatorial design of a highly efficient xylose-utilizing pathway in Saccharomyces cerevisiae for the production of cellulosic biofuels Appl. Environ. Microbiol. 79, 931-941 10.1128/AEM.02736-12
3. De Mey, M., Maertens, J., Lequeux, G. J., Soetaert, W. K., and Vandamme, E. J. (2007) Construction and model-based analysis of a promoter library for E. coli: an indispensable tool for metabolic engineering BMC Biotechnol. 7, 34 10.1186/1472-6750-7-34
4. Salis, H. M., Mirsky, E. A., and Voigt, C. A. (2009) Automated design of synthetic ribosome binding sites to control protein expression Nat. Biotechnol. 27, 946-950 10.1038/nbt.1568
5. Pfleger, B. F., Pitera, D. J., Smolke, C. D., and Keasling, J. D. (2006) Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes Nat. Biotechnol. 24, 1027-1032 10.1038/nbt1226
6. Si, T., Xiao, H., and Zhao, H. Rapid prototyping of microbial cell factories via genome-scale engineering, Biotechnol. Adv., 2014, DOI: 10.1016/j.biotechadv.2014.11.007
7. Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S., and Gregory, P. D. (2010) Genome editing with engineered zinc finger nucleases Nat. Rev. Genet. 11, 636-646 10.1038/nrg2842
8. Sun, N. and Zhao, H. (2013) Transcription activator-like effector nucleases (TALENs): A highly efficient and versatile tool for genome editing Biotechnol. Bioeng. 110, 1811-1821 10.1002/bit.24890
9. Na, D., Yoo, S. M., Chung, H., Park, H., Park, J. H., and Lee, S. Y. (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs Nat. Biotechnol. 31, 170-174 10.1038/nbt.2461
10. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., and Marraffini, L. A. (2013) Multiplex genome engineering using CRISPR/Cas systems Science 339, 819-823 10.1126/science.1231143
11. Linshiz, G., Stawski, N., Poust, S., Bi, C., Keasling, J. D., and Hillson, N. J. (2013) PaR-PaR laboratory automation platform ACS Synth. Biol. 2, 216-222 10.1021/sb300075t
12. Chao, R., Yuan, Y., and Zhao, H. (2014) Recent advances in DNA assembly technologies FEMS Yeast Res. 15, 1-9 10.1111/1567-1364.12171
13. Si, T., Luo, Y., Bao, Z., and Zhao, H. (2015) RNAi-assisted genome evolution in Saccharomyces cerevisiae for complex phenotype engineering ACS Synth. Biol. 4, 283-291 10.1021/sb500074a
14. DiCarlo, J. E., Conley, A. J., Penttilä, M., Jäntti, J., Wang, H. H., and Church, G. M. (2013) Yeast oligo-mediated genome engineering (YOGE) ACS Synth. Biol. 2, 741-749 10.1021/sb400117c
15. Dietrich, J. A., McKee, A. E., and Keasling, J. D. (2010) High-throughput metabolic engineering: advances in small-molecule screening and selection Annu. Rev. Biochem. 79, 563-590 10.1146/annurev-biochem-062608-095938
16. Becker, S., Schmoldt, H.-U., Adams, T. M., Wilhelm, S., and Kolmar, H. (2004) Ultra-high-throughput screening based on cell-surface display and fluorescence-activated cell sorting for the identification of novel biocatalysts Curr. Opin. Biotechnol. 15, 323-329 10.1016/j.copbio.2004.06.001
17. Zhang, F. and Keasling, J. (2011) Biosensors and their applications in microbial metabolic engineering Trends Microbiol. 19, 323-329 10.1016/j.tim.2011.05.003
18. Dietrich, J. A., Shis, D. L., Alikhani, A., and Keasling, J. D. (2013) Transcription factor-based screens and synthetic selections for microbial small-molecule biosynthesis ACS Synth. Biol. 2, 47-58 10.1021/sb300091d
19. Tang, S.-Y. and Cirino, P. C. (2011) Design and application of a mevalonate-responsive regulatory protein Angew. Chem., Int. Ed. 50, 1084-1086 10.1002/anie.201006083
20. Siedler, S., Stahlhut, S. G., Malla, S., Maury, J., and Neves, A. R. (2014) Novel biosensors based on flavonoid-responsive transcriptional regulators introduced into Escherichia coli Metab. Eng. 21, 2-8 10.1016/j.ymben.2013.10.011
21. Blount, B. A., Weenink, T., and Ellis, T. (2012) Construction of synthetic regulatory networks in yeast FEBS Lett. 586, 2112-2121 10.1016/j.febslet.2012.01.053
22. Herrgard, M. J., Covert, M. W., and Palsson, B. Ø. (2004) Reconstruction of microbial transcriptional regulatory networks Curr. Opin. Biotechnol. 15, 70-77 10.1016/j.copbio.2003.11.002
23. Umeyama, T., Okada, S., and Ito, T. (2013) Synthetic gene circuit-mediated monitoring of endogenous metabolites: identification of GAL11 as a novel multicopy enhancer of S-adenosylmethionine level in yeast ACS Synth. Biol. 2, 425-430 10.1021/sb300115n
24. Teo, W. S. and Chang, M. W. (2015) Bacterial XylRs and synthetic promoters function as genetically encoded xylose biosensors in Saccharomyces cerevisiae Biotechnol. J. 10, 315-322 10.1002/biot.201400159
25. Teo, W. S., Hee, K. S., and Chang, M. W. (2013) Bacterial FadR and synthetic promoters function as modular fatty acid sensor- regulators in Saccharomyces cerevisiae Eng. Life Sci. 13, 456-463 10.1002/elsc.201200113
26. Nevozhay, D., Zal, T., and Balázsi, G. (2013) Transferring a synthetic gene circuit from yeast to mammalian cells Nat. Commun. 4, 1451 10.1038/ncomms2471
27. Xu, P., Ranganathan, S., Fowler, Z. L., Maranas, C. D., and Koffas, M. A. (2011) Genome-scale metabolic network modeling results in minimal interventions that cooperatively force carbon flux towards malonyl-CoA Metab. Eng. 13, 578-587 10.1016/j.ymben.2011.06.008
28. Liu, T., Vora, H., and Khosla, C. (2010) Quantitative analysis and engineering of fatty acid biosynthesis in E. coli Metab. Eng. 12, 378-386 10.1016/j.ymben.2010.02.003
29. Gao, L., Chiou, W., Tang, H., Cheng, X., Camp, H. S., and Burns, D. J. (2007) Simultaneous quantification of malonyl-CoA and several other short-chain acyl-CoAs in animal tissues by ion-pairing reversed-phase HPLC/MS J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 853, 303-313 10.1016/j.jchromb.2007.03.029
30. López, M., Lelliott, C. J., Tovar, S., Kimber, W., Gallego, R., Virtue, S., Blount, M., Vázquez, M. J., Finer, N., and Powles, T. J. (2006) Tamoxifen-induced anorexia is associated with fatty acid synthase inhibition in the ventromedial nucleus of the hypothalamus and accumulation of malonyl-CoA Diabetes 55, 1327-1336 10.2337/db05-1356
31. Ellis, J. M. and Wolfgang, M. J. (2012) A genetically encoded metabolite sensor for malonyl-CoA Chem. Biol. 19, 1333-1339 10.1016/j.chembiol.2012.08.018
32. Schujman, G. E., Paoletti, L., Grossman, A. D., and de Mendoza, D. (2003) FapR, a bacterial transcription factor involved in global regulation of membrane lipid biosynthesis Dev. Cell 4, 663-672 10.1016/S1534-5807(03)00123-0
33. Schujman, G. E., Guerin, M., Buschiazzo, A., Schaeffer, F., Llarrull, L. I., Reh, G., Vila, A. J., Alzari, P. M., and De Mendoza, D. (2006) Structural basis of lipid biosynthesis regulation in Gram positive bacteria EMBO J. 25, 4074-4083 10.1038/sj.emboj.7601284
34. Xu, P., Wang, W., Li, L., Bhan, N., Zhang, F., and Koffas, M. A. (2014) Design and kinetic analysis of a hybrid promoter-regulator system for malonyl-CoA sensing in Escherichia coli ACS Chem. Biol. 9, 451-458 10.1021/cb400623m
35. Liu, D., Xiao, Y., Evans, B., and Zhang, F. (2015) Negative feedback regulation of fatty acid production based on a malonyl-CoA sensor-actuator ACS Synth. Biol. 4, 132-140 10.1021/sb400158w
36. Wang, M., Li, S., and Zhao, H. (2015) Design and engineering of intracellular-metabolite-sensing/regulation gene circuits in Saccharomyces cerevisiae Biotechnol. Bioeng. n/a 10.1002/bit.25676
37. Wattanachaisaereekul, S., Lantz, A. E., Nielsen, M. L., and Nielsen, J. (2008) Production of the polyketide 6-MSA in yeast engineered for increased malonyl-CoA supply Metab. Eng. 10, 246-254 10.1016/j.ymben.2008.04.005
38. Zhang, F., Carothers, J. M., and Keasling, J. D. (2012) Design of a dynamic sensor-regulator system for production of chemicals and fuels derived from fatty acids Nat. Biotechnol. 30, 354-359 10.1038/nbt.2149
39. Omura, S. (1976) The antibiotic cerulenin, a novel tool for biochemistry as an inhibitor of fatty acid synthesis Bacteriol. Rev. 40, 681
40. Suthers, P. F. and Cameron, D. C. Production of 3-hydroxypropionic acid in recombinant organisms, US Patent 6852517, 2005.
41. Rathnasingh, C., Raj, S. M., Lee, Y., Catherine, C., Ashok, S., and Park, S. (2012) Production of 3-hydroxypropionic acid via malonyl-CoA pathway using recombinant Escherichia coli strains J. Biotechnol. 157, 633-640 10.1016/j.jbiotec.2011.06.008
42. Chen, Y., Bao, J., Kim, I.-K., Siewers, V., and Nielsen, J. (2014) Coupled incremental precursor and co-factor supply improves 3-hydroxypropionic acid production in Saccharomyces cerevisiae Metab. Eng. 22, 104-109 10.1016/j.ymben.2014.01.005
43. 2 fixation J. Bacteriol. 184, 2404-2410 10.1128/JB.184.9.2404-2410.2002
44. +-ATPase of Saccharomyces cerevisiae J. Biol. Chem. 267, 6425-6428
45. Mousson, F., Coïc, Y.-M., Baleux, F., Beswick, V., Sanson, A., and Neumann, J.-M. (2002) Deciphering the role of individual acyl chains in the interaction network between phosphatidylserines and a single-spanning membrane protein Biochemistry 41, 13611-13616 10.1021/bi026274b
46. 2+-ATPases Nature 319, 689-693 10.1038/319689a0
47. Rogers, T. O. and Lichstein, H. C. (1969) Characterization of the biotin transport system in Saccharomyces cerevisiae J. Bacteriol. 100, 557-564
48. +-biotin symporter of Saccharomyces cerevisiae by rescue of a fatty acid-auxotrophic mutant J. Biol. Chem. 274, 18741-18746 10.1074/jbc.274.26.18741
49. Roggenkamp, R., Numa, S., and Schweizer, E. (1980) Fatty acid-requiring mutant of Saccharomyces cerevisiae defective in acetyl-CoA carboxylase Proc. Natl. Acad. Sci. U. S. A. 77, 1814-1817 10.1073/pnas.77.4.1814
50. Levert, K. L., Waldrop, G. L., and Stephens, J. M. (2002) A biotin analog inhibits acetyl-CoA carboxylase activity and adipogenesis J. Biol. Chem. 277, 16347-16350 10.1074/jbc.C200113200
51. Alber, T. and Kawasaki, G. (1981) Nucleotide sequence of the triose phosphate isomerase gene of Saccharomyces cerevisiae J. Mol. Appl. Genet. 1, 419-434
52. Compagno, C., Boschi, F., and Ranzi, B. M. (1996) Glycerol production in a triose phosphate isomerase deficient mutant of Saccharomyces cerevisiae Biotechnol. Prog. 12, 591-595 10.1021/bp960043c
53. Overkamp, K. M., Bakker, B. M., Kötter, P., Luttik, M. A. H., van Dijken, J. P., and Pronk, J. T. (2002) Metabolic engineering of glycerol production in Saccharomyces cerevisiae Appl. Environ. Microbiol. 68, 2814-2821 10.1128/AEM.68.6.2814-2821.2002
54. Shi, S., 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, e01130-01114 10.1128/mBio.01130-14
55. Jensen et al., Microbial production of 3-hydroxypropionic acid. Patent in application, 2013.
56. Shao, Z., Zhao, H., and Zhao, H. (2008) DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways Nucleic Acids Res. 37, e16 10.1093/nar/gkn991
57. Gietz, R. D., Schiestl, R. H., Willems, A. R., and Woods, R. A. (1995) Studies on the transformation of intact yeast-cells by the LiAc/s-DNA/PEG procedure Yeast 11, 355-360 10.1002/yea.320110408