13C metabolic flux analysis for systematic metabolic engineering of S. cerevisiae for overproduction of fatty acids

Frontiers in Bioengineering and Biotechnology

Volumn 4, Issue OCT, 2016, Pages

  Ghosh, Amit ^a,b,c   Ando, David ^a,b   Gin, Jennifer ^a,b   Runguphan, Weerawat ^a,b,d   Denby, Charles ^a,b   Wang, George ^a,b   Baidoo, Edward E K ^a,b   Shymansky, Chris ^a,b,e   Keasling, Jay D ^a,b,e,f,g   Martín, Héctor García ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b JOINT BIOENERGY INSTITUTE   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY   (India)

^d NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f University of California at Berkeley   (United States)

^g Chalmers University of Technology   (Denmark)

Author keywords

omics data; 13C metabolic flux analysis; Flux analysis; Metabolic engineering; Predictive biology

Indexed keywords

BIOCHEMISTRY; CARBON; CYTOLOGY; GENES; METABOLIC ENGINEERING; METABOLISM; PHYSIOLOGY; YEAST;

-OMICS DATA; FATTY ACID PRODUCTIONS; FLUX ANALYSIS; GENETIC MODIFICATIONS; METABOLIC FLUX ANALYSIS; MICROBIAL METABOLISM; PRODUCTION PATHWAYS; YARROWIA LIPOLYTICA;

FATTY ACIDS;

EID: 85032804740     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2016.00076     Document Type: Article

References (41)

1. Asadollahi, M. A., Maury, J., Patil, K. R., Schalk, M., Clark, A., and Nielsen, J. (2009). Enhancing sesquiterpene production in Saccharomyces cerevisiae through in silico driven metabolic engineering. Metab. Eng. 11, 328-334. doi:10.1016/j.ymben.2009.07.001
2. Bokinsky, G., Baidoo, E. E. K., Akella, S., Burd, H., Weaver, D., Alonso-Gutierrez, J., et al. (2013). HipA-triggered growth arrest and β-lactam tolerance in Escherichia coli are mediated by RelA-dependent ppGpp synthesis. J. Bacteriol. 195, 3173-3182. doi:10.1128/jb.02210-12
3. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., et al. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132. doi:10.1002/(sici)1097-0061(19980130)14:2<115:aid-yea204>3.0.co;2-2
4. Chen, J., Densmore, D., Ham, T. S., Keasling, J. D., and Hillson, N. J. (2012). DeviceEditor visual biological CAD canvas. J. Biol. Eng. 6, 1. doi:10.1186/preaccept-1967068768635731
5. Chen, Y., Daviet, L., Schalk, M., Siewers, V., and Nielsen, J. (2013). Establishing a platform cell factory through engineering of yeast acetyl-CoA metabolism. Metab. Eng. 15, 48-54. doi:10.1016/j.ymben.2012.11.002
6. Fjerbaek, L., Christensen, K. V., and Norddahl, B. (2009). A review of the current state of biodiesel production using enzymatic transesterification. Biotechnol. Bioeng. 102, 1298-1315. doi:10.1002/bit.22256
7. Fortman, J., Chhabra, S., Mukhopadhyay, A., Chou, H., Lee, T. S., Steen, E., et al. (2008). Biofuel alternatives to ethanol: pumping the microbial well. Trends Biotechnol. 26, 375-381. doi:10.1016/j.tibtech.2008.03.008
8. Gietz, R. D., and Woods, R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96. doi:10.1016/S0076-6879(02)50957-5
9. Goh, E.-B., Baidoo, E. E., Burd, H., Lee, T. S., Keasling, J. D., and Beller, H. R. (2014). Substantial improvements in methyl ketone production in E. coli and insights on the pathway from in vitro studies. Metab. Eng. 26, 67-76. doi:10.1016/j.ymben.2014.09.003
10. Goldstein, A. L., and McCusker, J. H. (1999). Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553. doi:10.1002/(sici)1097-0061(199910)15:14<1541:aid-yea476>3.0.co;2-k
11. Gopalakrishnan, S., and Maranas, C. (2015b). Achieving metabolic flux analysis for S. cerevisiae at a genome-scale: challenges requirements, and considerations. Metabolites 5, 521-535. doi:10.3390/metabo5030521
12. Gopalakrishnan, S., and Maranas, C. D. (2015a). 13C metabolic flux analysis at a genome-scale. Metab. Eng. 32, 12-22. doi:10.1016/j.ymben.2015.08.006
13. Ham, T. S., Dmytriv, Z., Plahar, H., Chen, J., Hillson, N. J., and Keasling, J. D. (2012). Design implementation and practice of JBEI-ICE: an open source biological part registry platform and tools. Nucleic Acids Res. 40, e141-e141. doi:10.1093/nar/gks531
14. Hillson, N. J., Rosengarten, R. D., and Keasling, J. D. (2012). j5 DNA assembly design automation software. ACS Synth. Biol. 1, 14-21. doi:10.1021/sb2000116
15. Kajihata, S., Matsuda, F., Yoshimi, M., Hayakawa, K., Furusawa, C., Kanda, A., et al. (2015). 13C-based metabolic flux analysis of Saccharomyces cerevisiae with a reduced crabtree effect. J. Biosci. Bioeng. 120, 140-144. doi:10.1016/j.jbiosc.2014.12.014
16. Keasling, J. D., and Chou, H. (2008). Metabolic engineering delivers next-generation biofuels. Nat. Biotechnol. 26, 298-299. doi:10.1038/nbt0308-298
17. Kocharin, K., Chen, Y., Siewers, V., and Nielsen, J. (2012). Engineering of acetyl-CoA metabolism for the improved production of polyhydroxybutyrate in Saccharomyces cerevisiae. AMB Exp. 2, 52. doi:10.1186/2191-0855-2-52
18. Kozak, B. U., van Rossum, H. M., Luttik, M. A. H., Akeroyd, M., Benjamin, K. R., Wu, L., et al. (2014). Engineering acetyl coenzyme a supply: functional expression of a bacterial pyruvate dehydrogenase complex in the cytosol of Saccharomyces cerevisiae. MBio 5, e1696-e1614. doi:10.1128/mbio.01696-14
19. Krivoruchko, A., Serrano-Amatriain, C., Chen, Y., Siewers, V., and Nielsen, J. (2013). Improving biobutanol production in engineered Saccharomyces cerevisiae by manipulation of acetyl-CoA metabolism. J. Ind. Microbiol. Biotechnol. 40, 1051-1056. doi:10.1007/s10295-013-1296-0
20. Lian, J., Si, T., Nair, N. U., and Zhao, H. (2014). Design and construction of acetyl-CoA overproducing Saccharomyces cerevisiae strains. Metab. Eng. 24, 139-149. doi:10.1016/j.ymben.2014.05.010
21. Martín, H. G., Kumar, V. S., Weaver, D., Ghosh, A., Chubukov, V., Mukhopadhyay, A., et al. (2015). A method to constrain genome-scale models with 13C labeling data. PLoS Comput. Biol. 11:e1004363. doi:10.1371/journal.pcbi.1004363
22. Mo, M. L., Palsson, B. Ø, and Herrgård, M. J. (2009). Connecting extracellular metabolomic measurements to intracellular flux states in yeast. BMC Syst. Biol. 3:37. doi:10.1186/1752-0509-3-37
23. Moxley, J. F., Jewett, M. C., Antoniewicz, M. R., Villas-Boas, S. G., Alper, H., Wheeler, R. T., et al. (2009). Linking high-resolution metabolic flux phenotypes and transcriptional regulation in yeast modulated by the global regulator Gcn4p. Proc. Natl. Acad. Sci. U.S.A. 106, 6477-6482. doi:10.1073/pnas.0811091106
24. Naik, S., Goud, V. V., Rout, P. K., and Dalai, A. K. (2010). Production of first and second generation biofuels: a comprehensive review. Renew. Sust. Energ. Rev. 14, 578-597. doi:10.1016/j.rser.2009.10.003
25. Nevoigt, E., Kohnke, J., Fischer, C. R., Alper, H., Stahl, U., and Stephanopoulos, G. (2006). Engineering of promoter replacement cassettes for fine-tuning of gene expression in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 72, 5266-5273. doi:10.1128/aem.00530-06
26. Papanikolaou, S., Chevalot, I., Komaitis, M., Marc, I., and Aggelis, G. (2002). Single cell oil production by Yarrowia lipolytica growing on an industrial derivative of animal fat in batch cultures. Appl. Microbiol. Biotechnol. 58, 308-312. doi:10.1007/s00253-001-0897-0
27. Park, J. M., Kim, T. Y., and Lee, S. Y. (2009). Constraints-based genome-scale metabolic simulation for systems metabolic engineering. Biotechnol. Adv. 27, 979-988. doi:10.1016/j.biotechadv.2009.05.019
28. Perez, F., and Granger, B. E. (2007). IPython: a system for interactive scientific computing. Comput. Sci. Eng. 9, 21-29. doi:10.1109/mcse.2007.53
29. Regenberg, B., Grotkjaer, T., Winther, O., Fausball, A., Akesson, M., Bro, C., et al. (2006). Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae. Genome Biol. 7, R107. doi:10.1186/gb-2006-7-4-107
30. Rodriguez, S., Denby, C. M., Vu, T. V., Baidoo, E. E. K., Wang, G., and Keasling, J. D. (2016). ATP citrate lyase mediated cytosolic acetyl-CoA biosynthesis increases mevalonate production in Saccharomyces cerevisiae. Microb. Cell Fact. 15, 48. doi:10.1186/s12934-016-0447-1
31. Runguphan, W., and Keasling, J. D. (2014). Metabolic engineering of Saccharomyces cerevisiae for production of fatty acid-derived biofuels and chemicals. Metab. Eng. 21, 103-113. doi:10.1016/j.ymben.2013.07.003
32. Schellenberger, J., Park, J. O., Conrad, T. M., and Palsson, B. Ø (2010). BiGG: a biochemical genetic and genomic knowledgebase of large scale metabolic reconstructions. BMC Bioinformatics 11:213. doi:10.1186/1471-2105-11-213
33. 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
34. Shiba, Y., Paradise, E. M., Kirby, J., Ro, D.-K., and Keasling, J. D. (2007). Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab. Eng. 9, 160-168. doi:10.1016/j.ymben.2006.10.005
35. Sims, R. E., Mabee, W., Saddler, J. N., and Taylor, M. (2010). An overview of second generation biofuel technologies. Bioresour. Technol. 101, 1570-1580. doi:10.1016/j.biortech.2009.11.046
36. Steen, E. J., Kang, Y., Bokinsky, G., Hu, Z., Schirmer, A., McClure, A., et al. (2010a). Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463, 559-562. doi:10.1038/nature08721
37. Steen, E., Kang, Y., Bokinsky, G., Hu, Z., Schirmer, A., McClure, A., et al. (2010b). Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463, 559-562. doi:10.1038/nature08721
38. Thiele, I., and Palsson, B. Ø (2010). A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat. Protoc. 5, 93-121. doi:10.1038/nprot.2009.203
39. Van, H. P., Van, D. J., and Pronk, J. (1998). Effect of specific growth rate on fermentative capacity of baker's yeast. Appl. Environ. Microbiol. 64, 4226-4233
40. Voeste, T., and Buchold, H. (1984). Production of fatty alcohols from fatty acids. J. Am. Oil Chem. Soc. 61, 350-352. doi:10.1007/bf02678794
41. Zhou, Y. J., Buijs, N. A., Zhu, Z., Qin, J., Siewers, V., and Nielsen, J. (2016). Production of fatty acid-derived oleochemicals and biofuels by synthetic yeast cell factories. Nat. Commun. 7, 11709. doi:10.1038/ncomms11709