Engineering high-level production of fatty alcohols by Saccharomyces cerevisiae from lignocellulosic feedstocks

Metabolic Engineering

Volumn 42, Issue , 2017, Pages 115-125

  d'Espaux, Leo ^a,b   Ghosh, Amit ^a,b,g   Runguphan, Weerawat ^a,b,h   Wehrs, Maren ^a,b   Xu, Feng ^a,b,c   Konzock, Oliver ^a,b   Dev, Ishaan ^a,b,d   Nhan, Melissa ^a,b,i   Gin, Jennifer ^a,b   Reider Apel, Amanda ^a,b   Petzold, Christopher J ^a,b   Singh, Seema ^a,b,c   Simmons, Blake A ^a,b,c   Mukhopadhyay, Aindrila ^a,b   García Martín, Héctor ^a,b   Keasling, Jay D ^a,b,d,e,f  

^a JOINT BIOENERGY INSTITUTE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c SANDIA NATIONAL LABORATORIES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of California   (United States)

^f TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^g INDIAN INSTITUTE OF TECHNOLOGY   (India)

^h NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

ⁱ Calysta Energy   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOLS; BOTTLES; CARBON; CELL MEMBRANES; FEEDSTOCKS; GENE EXPRESSION; GLUCOSE; IONIC LIQUIDS; YEAST;

ACETYL-COA CARBOXYLASE; ENDOPLASMIC RETICULUM; FED-BATCH FERMENTATION; GLUTAMATE DEHYDROGENASE; HIGH-LEVEL PRODUCTION; LIGNOCELLULOSIC FEEDSTOCKS; MICROBIAL PRODUCTION; PERSONAL CARE PRODUCTS;

FATTY ACIDS;

ACETALDEHYDE; ACETYL COENZYME A; ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A; ACYL COENZYME A STEROL ACYLTRANSFERASE; ACYLTRANSFERASE; ADH6 PROTEIN; ALCOHOL DEHYDROGENASE; ALCOHOL DEHYDROGENASE (ETHANOL FORMING NAD DEPENDENT); ALDEHYDE DEHYDROGENASE (CYTOSOLIC NADP DEPENDENT; CARBON; DGA1 PROTEIN; DIACYLGLYCEROL ACYLTRANSFERASE; FATTY ACID; FATTY ACID REDUCTASE; FATTY ACID REDUCTASE (FATTY ACYL COENZYME A REDUCTASE, NADPH DEPENDENT); FATTY ACID SYNTHASE; FATTY ALCOHOL; GLUCOSE; GLUCOSE 6 PHOSPHATE; GLUTAMATE DEHYDROGENASE; GLYCERALDEHYDE 3 PHOSPHATE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HFD1 PROTEIN; IONIC LIQUID; LIGNOCELLULOSE; OLE1 PROTEIN; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG; ACYL COENZYME A DESATURASE; ADH6 PROTEIN, S CEREVISIAE; ALDEHYDE DEHYDROGENASE; DELTA-9 FATTY ACID DESATURASE; DGA1 PROTEIN, S CEREVISIAE; LIGNIN; RECOMBINANT PROTEIN;

ARTICLE; BATCH REACTOR; BIOTECHNOLOGICAL PRODUCTION; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ENGINEERING; ENZYME LOCALIZATION; FATTY ACID SYNTHESIS; FED BATCH FERMENTATION; FUNGAL STRAIN; GENE EDITING; METABOLISM; MOUSE; MUS MUSCULUS; NONHUMAN; PANICUM VIRGATUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE; SORGHUM; ANIMAL; GENE DELETION; GENETICS; METABOLIC ENGINEERING;

ALCOHOL DEHYDROGENASE; ALDEHYDE OXIDOREDUCTASES; ANIMALS; DIACYLGLYCEROL O-ACYLTRANSFERASE; FATTY ALCOHOLS; GENE DELETION; LIGNIN; METABOLIC ENGINEERING; MICE; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STEAROYL-COA DESATURASE;

EID: 85020547969     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2017.06.004     Document Type: Article

References (50)

1. Avalos, J.L., Fink, G.R., Stephanopoulos, G., Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat. Biotechnol. 31 (2013), 335–341, 10.1038/nbt.2509.
2. Batth, T.S., Keasling, J.D., Petzold, C.J., 2012. Targeted proteomics for metabolic pathway optimization. In: Fungal Secondary Metabolism: Methods and Protocols, Methods in Molecular Biology. Vol. 944. pp. 47–58. http://dx.doi.org/10.1007/978-1-62703-122-6.
3. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., Boeke, J.D., 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 (1998), 115–132, 10.1002/(SICI)1097-0061(19980130)14:2 < 115::AID-YEA204>3.0.CO;2-2.
4. Caspeta, L., Nielsen, J., Economic and environmental impacts of microbial biodiesel. Nat. Biotechnol. 31 (2013), 789–793, 10.1038/nbt.2683.
5. Clomburg, J.M., Blankschien, M.D., Vick, J.E., Chou, A., Kim, S., Gonzalez, R., Integrated engineering of β-oxidation reversal and ω-oxidation pathways for the synthesis of medium chain ω-functionalized carboxylic acids. Metab. Eng. 28 (2015), 202–212, 10.1016/j.ymben.2015.01.007.
6. Connor, R., Uhlenbrook, S., 2016. The United Nations World Water Development Report 2016. Paris, France.
7. Degreif, D., de Rond, T., Bertl, A., Keasling, J.D., Budin, I., Lipid engineering reveals regulatory roles for membrane fluidity in yeast flocculation and oxygen-limited growth. Metab. Eng. 41 (2017), 46–56, 10.1016/j.ymben.2017.03.002.
8. Feng, X., Lian, J., Zhao, H., Metabolic engineering of Saccharomyces cerevisiae to improve 1-hexadecanol production. Metab. Eng. 27 (2015), 10–19, 10.1016/j.ymben.2014.10.001.
9. Fillet, S., Gibert, J., Suárez, B., Lara, A., Ronchel, C., Adrio, J.L., Fatty alcohols production by oleaginous yeast. J. Ind. Microbiol. Biotechnol. 42 (2015), 1463–1472, 10.1007/s10295-015-1674-x.
10. Gaikwad, S., 2016. Fatty Alcohol Market Size, Industry Analysis Report: Forecast, 2016–2023. Ocean View, DE.
11. García Martín, H., Kumar, V.S., Weaver, D., Ghosh, A., Chubukov, V., Mukhopadhyay, A., Arkin, A., Keasling, J.D., A method to constrain genome-scale models with 13C labeling data. PLOS Comput. Biol., 11, 2015, e1004363, 10.1371/journal.pcbi.1004363.
12. Ghosh, A., Ando, D., Gin, J., Runguphan, W., Denby, C., Wang, G., Baidoo, E.E.K., Shymansky, C., Keasling, J.D., García Martín, H., (13)C metabolic flux analysis for systematic metabolic engineering of S. cerevisiae for overproduction of fatty acids. Front. Bioeng. Biotechnol., 4, 2016, 76, 10.3389/fbioe.2016.00076.
13. Gietz, R.D., Woods, R.A., Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350 (2002), 87–96.
14. Goh, E.-B., Baidoo, E.E.K., Keasling, J.D., Beller, H.R., Engineering of bacterial methyl ketone synthesis for biofuels. Appl. Environ. Microbiol. 78 (2012), 70–80, 10.1128/AEM.06785-11.
15. Guo, Z., Zhang, L., Ding, Z., Shi, G., Minimization of glycerol synthesis in industrial ethanol yeast without influencing its fermentation performance. Metab. Eng. 13 (2011), 49–59, 10.1016/j.ymben.2010.11.003.
16. Haushalter, R.W., Kim, W., Chavkin, T.A., The, L., Garber, M.E., Nhan, M., Adams, P.D., Petzold, C.J., Katz, L., Keasling, J.D., Production of anteiso-branched fatty acids in Escherichia coli; next generation biofuels with improved cold-flow properties. Metab. Eng. 26C (2014), 111–118, 10.1016/j.ymben.2014.09.002.
17. Hoja, U., Marthol, S., Hofmann, J., Stegner, S., Schulz, R., Meier, S., Greiner, E., Schweizer, E., HFA1 encoding an organelle-specific acetyl-CoA carboxylase controls mitochondrial fatty acid synthesis in Saccharomyces cerevisiae. J. Biol. Chem. 279 (2004), 21779–21786, 10.1074/jbc.M401071200.
18. Kalscheuer, R., Stölting, T., Steinbüchel, A., Microdiesel: Escherichia coli engineered for fuel production. Microbiology 152 (2006), 2529–2536, 10.1099/mic.0.29028-0.
19. Kildegaard, K.R., Jensen, N.B., Schneider, K., Czarnotta, E., Ozdemir, E., Klein, T., Maury, J., Ebert, B.E., Christensen, H.B., Chen, Y., Kim, I.K., Herrgard, M.J., Blank, L.M., Forster, J., Nielsen, J., Borodina, I., Engineering and systems-level analysis of Saccharomyces cerevisiae for production of 3-hydroxypropionic acid via malonyl-CoA reductase-dependent pathway. Microb. Cell Fact., 15, 2016, 13, 10.1186/s12934-016-0451-5.
20. Lee, M.E., DeLoache, W.C., Cervantes, B., Dueber, J.E., A highly-characterized yeast toolkit for modular, multi-part assembly. ACS Synth. Biol., 2015, 10.1021/sb500366v.
21. Liu, A., Tan, X., Yao, L., Lu, X., Fatty alcohol production in engineered E. coli expressing Marinobacter fatty acyl-CoA reductases. Appl. Microbiol. Biotechnol. 97 (2013), 7061–7071, 10.1007/s00253-013-5027-2.
22. Liu, Y., Chen, S., Chen, J., Zhou, J., Wang, Y., Yang, M., Qi, X., Xing, J., Wang, Q., Ma, Y., High production of fatty alcohols in Escherichia coli with fatty acid starvation. Microb. Cell Fact., 15, 2016, 129, 10.1186/s12934-016-0524-5.
23. Mazzoleni, S., Landi, C., Cartenì, F., de Alteriis, E., Giannino, F., Paciello, L., Parascandola, P., A novel process-based model of microbial growth: self-inhibition in Saccharomyces cerevisiae aerobic fed-batch cultures. Microb. Cell Fact., 14, 2015, 109, 10.1186/s12934-015-0295-4.
24. Mo, M.L., Palsson, B.Ø., Herrgård, M.J., Connecting extracellular metabolomic measurements to intracellular flux states in yeast. BMC Syst. Biol., 3, 2009, 37, 10.1186/1752-0509-3-37.
25. Montague, T.G., Cruz, J.M., Gagnon, J.A., Church, G.M., Valen, E., CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 42 (2014), 401–407, 10.1093/nar/gku410.
26. Natter, K., Leitner, P., Faschinger, A., Wolinski, H., McCraith, S., Fields, S., Kohlwein, S.D., The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy. Mol. Cell. Proteom. 4 (2005), 662–672, 10.1074/mcp.M400123-MCP200.
27. Petkovic, M., Ferguson, J.L., Gunaratne, H.Q.N., Ferreira, R., Leitão, M.C., Seddon, K.R., Rebelo, L.P.N., Pereira, C.S., Pereira, C.S., Ferreira, R., Seddon, K.R., Rebelo, L.P.N., Pereira, C.S., Novel biocompatible cholinium-based ionic liquids—toxicity and biodegradability. Green Chem., 12, 2010, 643, 10.1039/b922247b.
28. Pfleger, B.F., Gossing, M., Nielsen, J., Metabolic engineering strategies for microbial synthesis of oleochemicals. Metab. Eng. 29 (2015), 1–11, 10.1016/j.ymben.2015.01.009.
29. Qiao, K., Imam Abidi, S.H., Liu, H., Zhang, H., Chakraborty, S., Watson, N., Kumaran Ajikumar, P., Stephanopoulos, G., Engineering lipid overproduction in the oleaginous yeast Yarrowia lipolytica. Metab. Eng. 29 (2015), 56–65, 10.1016/j.ymben.2015.02.005.
30. Reider Apel, A., D'Espaux, L., Wehrs, M., Sachs, D., Li, R.A., Tong, G.J., Garber, M., Nnadi, O., Zhuang, W., Hillson, N.J., Keasling, J.D., Mukhopadhyay, A., A Cas9-based toolkit to program gene expression in Saccharomyces cerevisiae. Nucleic Acids Res., 2016, 1–14, 10.1093/gbe/evw245.
31. Runguphan, W., Keasling, J.D., Metabolic engineering of saccharomyces cerevisiae for production of fatty acid-derived biofuels and chemicals. Metab. Eng. 21 (2013), 103–113, 10.1016/j.ymben.2013.07.003.
32. Sheng, J., Stevens, J., Feng, X., Pathway compartmentalization in peroxisome of Saccharomyces cerevisiae to produce versatile medium chain fatty alcohols. Nat. Publ. Gr., 2016, 10.1038/srep26884.
33. Shi, S., Chen, Y., Siewers, V., Improving production of malonyl coenzyme A-derived metabolites. mBio 5 (2014), e01130–14, 10.1128/mBio.01130-14.Editor.
34. Stryer, L., 1988. Biochemistry. W.H. Freeman.
35. 2 enabled process integration for the production of cellulosic ethanol using bionic liquids. Energy Environ. Sci. 9 (2016), 2822–2834, 10.1039/C6EE00913A.
36. Tai, M., Stephanopoulos, G., Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab. Eng. 15 (2013), 1–9, 10.1016/j.ymben.2012.08.007.
37. Tehlivets, O., Scheuringer, K., Kohlwein, S.D., Fatty acid synthesis and elongation in yeast. Biochim. Biophys. Acta 1771 (2007), 255–270, 10.1016/j.bbalip.2006.07.004.
38. Teixeira, P.G., Ferreira, R., Zhou, Y.J., Siewers, V., Nielsen, J., Dynamic regulation of fatty acid pools for improved production of fatty alcohols in Saccharomyces cerevisiae. Microb. Cell Fact., 2017, 1–11, 10.1186/s12934-017-0663-3.
39. Thomas, D., Cherest, H., Surdin-Kerjan, Y., Identification of the structural gene for glucose-6-phosphate dehydrogenase in yeast. Inactivation leads to a nutritional requirement for organic sulfur. EMBO J. 10 (1991), 547–553.
40. Verho, R., Richard, P., Jonson, P.H., Sundqvist, L., Londesborough, J., Penttilä, M., Identification of the first fungal NADP-GAPDH from Kluyveromyces lactis. Biochemistry 41 (2002), 13833–13838, 10.1021/bi0265325.
41. Wahlen, B.D., Oswald, W.S., Seefeldt, L.C., Barney, B.M., Purification, characterization, and potential bacterial wax production role of an NADPH-dependent fatty aldehyde reductase from Marinobacter aquaeolei VT8. Appl. Environ. Microbiol. 75 (2009), 2758–2764, 10.1128/AEM.02578-08.
42. Wang, G., Xiong, X., Ghogare, R., Wang, P., Meng, Y., Chen, S., Biotechnology for biofuels exploring fatty alcohol – producing capability of Yarrowia lipolytica. Biotechnol. Biofuels, 2016, 1–10, 10.1186/s13068-016-0512-3.
43. Willis, R.M., Wahlen, B.D., Seefeldt, L.C., Barney, B.M., Characterization of a fatty acyl-CoA reductase from Marinobacter aquaeolei VT8: a bacterial enzyme catalyzing the reduction of fatty acyl-CoA to fatty alcohol. Biochemistry 50 (2011), 10550–10558, 10.1021/bi2008646.
44. Xu, F., Sun, J., Konda, N.V.S.N.M., Shi, J., Dutta, T., Scown, C.D., Simmons, B.A., Singh, S., Transforming biomass conversion with ionic liquids: process intensification and the development of a high-gravity, one-pot process for the production of cellulosic ethanol. Energy Environ. Sci. 9 (2016), 1042–1049, 10.1039/C5EE02940F.
45. Xu, P., Qiao, K., Suk, W., Stephanopoulos, G., 2016. Engineering Yarrowia Lipolytica as a Platform for Synthesis of Drop-in Transportation Fuels and Oleochemicals. 113. http://dx.doi.org/10.1073/pnas.1607295113.
46. Zampar, G.G., Kümmel, A., Ewald, J., Jol, S., Niebel, B., Picotti, P., Aebersold, R., Sauer, U., Zamboni, N., Heinemann, M., Temporal system-level organization of the switch from glycolytic to gluconeogenic operation in yeast. Mol. Syst. Biol., 9, 2013, 651, 10.1038/msb.2013.11.
47. Zhang, F., Ouellet, M., Batth, T.S., Adams, P.D., Petzold, C.J., Mukhopadhyay, A., Keasling, J.D., Enhancing fatty acid production by the expression of the regulatory transcription factor FadR. Metab. Eng. 14 (2012), 653–660, 10.1016/j.ymben.2012.08.009.
48. Zhang, L., Tang, Y., Guo, Z., Ding, Z., Shi, G., Improving the ethanol yield by reducing glycerol formation using cofactor regulation in Saccharomyces cerevisiae. Biotechnol. Lett. 33 (2011), 1375–1380, 10.1007/s10529-011-0588-6.
49. Zhou, Y.J., Buijs, N.A., Zhu, Z., Qin, J., Siewers, V., Nielsen, J., Production of fatty acid-derived oleochemicals and biofuels by synthetic yeast cell factories. Nat. Commun., 7, 2016, 11709, 10.1038/ncomms11709.
50. Zhu, S., Wu, Y., Chen, Q., Yu, Z., Wang, C., Jin, S., Ding, Y., Wu, G., Tu, S., Xue, Y., Dissolution of cellulose with ionic liquids and its application: a mini-review. Green Chem., 8, 2006, 325, 10.1039/b601395c.