A metabolic engineering strategy for producing free fatty acids by the Yarrowia lipolytica yeast based on impairment of glycerol metabolism

Biotechnology and Bioengineering

Volumn 115, Issue 2, 2018, Pages 433-443

  Yuzbasheva, Evgeniya Y ^a   Mostova, Elizaveta B ^a   Andreeva, Natalia I ^a   Yuzbashev, Tigran V ^a   Fedorov, Alexander S ^a   Konova, Irina A ^b   Sineoky, Sergey P ^a  

^a STATE RESEARCH INSTITUTE OF GENETICS AND SELECTION OF INDUSTRIAL MICROORGANISMS   (Russian Federation)

^b KURCHATOV INSTITUTE   (Russian Federation)

Author keywords

free fatty acid production; growth repression by glycerol; impaired glycerol metabolism; metabolic engineering; oleate toxicity

Indexed keywords

CYTOLOGY; GLUCOSE; GLYCEROL; METABOLIC ENGINEERING; METABOLISM; TOXICITY; YEAST;

BIOFUELS AND BIOCHEMICALS; BIOMASS ACCUMULATION; FREE FATTY ACID; GENETIC BACKGROUNDS; GLUCOSE CONSUMPTION; PEROXISOME BIOGENESIS; SUBSTRATE UTILIZATION; YARROWIA LIPOLYTICA;

FATTY ACIDS;

DODECANE; FATTY ACID; GLUCOSE; GLYCEROL; OLEIC ACID;

ACC1 GENE; ALCOHOL METABOLISM; ARTICLE; BIOMASS; CONTROLLED STUDY; FATTY ACID SYNTHESIS; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE OVEREXPRESSION; GENETIC BACKGROUND; GLUCOSE INTAKE; GLUCOSE UTILIZATION; GROWTH INHIBITION; METABOLIC ENGINEERING; NONHUMAN; ORGANELLE BIOGENESIS; PEROXISOME; TEST TUBE; UPREGULATION; YARROWIA LIPOLYTICA; CELL PROLIFERATION; DRUG EFFECT; GENETICS; METABOLISM; PROCEDURES; YARROWIA;

CELL PROLIFERATION; FATTY ACIDS, NONESTERIFIED; GLUCOSE; GLYCEROL; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; OLEIC ACID; YARROWIA;

EID: 85032884347     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.26402     Document Type: Article

References (47)

1. Beopoulos, A, Haddouche, R, Kabran, P, Dulermo, T, Chardot, T, & Nicaud, JM. (2012). Identification and characterization of DGA2, an acyltransferase of the DGAT1 acyl-CoA:diacylglycerol acyltransferase family in the oleaginous yeast Yarrowia lipolytica. New insights into the storage lipid metabolism of oleaginous yeasts. Applied Microbiology and Biotechnology, 93(4), 1523–1537.
2. Beopoulos, A, Nicaud, JM, & Gaillardin, C. (2011). An overview of lipid metabolism in yeasts and its impact on biotechnological processes. Applied Microbiology and Biotechnology, 90(4), 1193–1206.
3. Cozzarelli, NR, Koch, JP, Hayashi, S, & Lin, EC. (1965). Growth stasis by accumulated L-alpha-glycerophosphate in Escherichia coli. Journal of Bacteriology, 90(5), 1325–1329.
4. d'Espaux, L, Mendez-Perez, D, Li, R, & Keasling, JD. (2015). Synthetic biology for microbial production of lipid-based biofuels. Current Opinion in Chemical Biology, 29, 58–65.
5. Desbois, AP, & Smith, VJ. (2010). Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Applied Microbiology and Biotechnology, 85(6), 1629–1642.
6. Englesberg, E, Anderson, RL, Weinberg, R, Lee, N, Hoffee, P, Huttenhauer, G, & Boyer, H. (1962). L-Arabinose-sensitive, L-ribulose 5-phosphate 4-epimerase-deficient mutants of Escherichia coli. Journal of Bacteriology, 84, 137–146.
7. Eppler, T, & Boos, W. (1999). Glycerol-3-phosphate-mediated repression of malT in Escherichia coli does not require metabolism, depends on enzyme IIAGlc and is mediated by cAMP levels. Molecular Microbiology, 33(6), 1221–1231.
8. Fernandez-Moya, R, Leber, C, Cardenas, J, & Da Silva, NA. (2015). Functional replacement of the Saccharomyces cerevisiae fatty acid synthase with a bacterial type II system allows flexible product profiles. Biotechnology and Bioengineering, 112(12), 2618–2623.
9. Folch, J, Lees, M, & Sloane Stanley, GH (1957). A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry, 226(1), 497–509.
10. Huang, C, Chen, XF, Xiong, L, Chen, XD, Ma, LL, & Chen, Y. (2013). Single cell oil production from low-cost substrates: The possibility and potential of its industrialization. Biotechnology Advances, 31(2), 129–139.
11. Ilic-Tomic, T, Gencic, MS, Zivkovic, MZ, Vasiljevic, B, Djokic, L, Nikodinovic-Runic, J, & Radulovic, NS. (2015). Structural diversity and possible functional roles of free fatty acids of the novel soil isolate Streptomyces sp. NP10. Applied Microbiology and Biotechnology, 99(11), 4815–4833.
12. Kallio, P, Pasztor, A, Akhtar, MK, & Jones, PR. (2014). Renewable jet fuel. Current Opin. Biotechnol., 26, 50–55.
13. Katayama, T, Kanno, M, Morita, N, Hori, T, Narihiro, T, Mitani, Y, & Kamagata, Y. (2014). An oleaginous bacterium that intrinsically accumulates long-chain free fatty acids in its cytoplasm. Applied and Environmental Microbiology, 80(3), 1126–1131.
14. Leber, C, & Da Silva, NA. (2014). Engineering of Saccharomyces cerevisiae for the synthesis of short chain fatty acids. Biotechnology and Bioengineering, 111(2), 347–358.
15. Leber, C, Polson, B, Fernandez-Moya, R, & Da Silva, NA. (2015). Overproduction and secretion of free fatty acids through disrupted neutral lipid recycle in Saccharomyces cerevisiae. Metabolic Engineering, 28, 54–62.
16. Ledesma-Amaro, R, Dulermo, R, Niehus, X, & Nicaud, JM. (2016). Combining metabolic engineering and process optimization to improve production and secretion of fatty acids. Metabolic Engineering, 38, 38–46.
17. Leibundgut, M, Maier, T, Jenni, S, & Ban, N. (2008). The multienzyme architecture of eukaryotic fatty acid synthases. Current Opinion in Structural Biology, 18(6), 714–725.
18. Leman, J. (1997). Oleaginous microorganisms: An assessment of the potential. Advances in Applied Microbiology, 43, 195–243.
19. Lennen, RM, Kruziki, MA, Kumar, K, Zinkel, RA, Burnum, KE, Lipton, MS, … Marner, WD (2011). Membrane stresses induced by overproduction of free fatty acids in Escherichia coli. Applied and Environmental Microbiology, 77(22), 8114–8128.
20. Lennen, RM, & Pfleger, BF. (2012). Engineering Escherichia coli to synthesize free fatty acids. Trends in Biotechnology, 30(12), 659–667.
21. Lian, J, & Zhao, H. (2015). Recent advances in biosynthesis of fatty acids derived products in Saccharomyces cerevisiae via enhanced supply of precursor metabolites. Journal of Industrial Microbiology & Biotechnology, 42(3), 437–451.
22. Lockshon, D, Surface, LE, Kerr, EO, Kaeberlein, M, & Kennedy, BK. (2007). The sensitivity of yeast mutants to oleic acid implicates the peroxisome and other processes in membrane function. Genetics, 175(1), 77–91.
23. Lu, X, Vora, H, & Khosla, C. (2008). Overproduction of free fatty acids in E. coli: implications for biodiesel production. Metabolic Engineering, 10(6), 333–339.
24. Michinaka, Y, Shimauchi, T, Aki, T, Nakajima, T, Kawamoto, S, Shigeta, S, … Ono, K. (2003). Extracellular secretion of free fatty acids by disruption of a fatty acyl-CoA synthetase gene in Saccharomyces cerevisiae. Journal of Bioscience and Bioengineering, 95(5), 435–440.
25. Mori, K, Iwama, R, Kobayashi, S, Horiuchi, H, Fukuda, R, & Ohta, A. (2013). Transcriptional repression by glycerol of genes involved in the assimilation of n-alkanes and fatty acids in yeast Yarrowia lipolytica. FEMS Yeast Research, 13(2), 233–240.
26. Ramos, MJ, Fernandez, CM, Casas, A, Rodriguez, L, & Perez, A. (2009). Influence of fatty acid composition of raw materials on biodiesel properties. Bioresource Technol, 100(1), 261–268.
27. Ruffing, AM. (2014). Improved free fatty acid production in cyanobacteria with Synechococcus sp. PCC 7002 as host. Frontiers in Bioengineering and Biotechnology, 2, 17.
28. Runguphan, W, & Keasling, JD. (2014). Metabolic engineering of Saccharomyces cerevisiae for production of fatty acid-derived biofuels and chemicals. Metabolic Engineering, 21, 103–113.
29. Sambrook, J, Maniatis, T, & Fritsch, E. (1989). Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.
30. Scharnewski, M, Pongdontri, P, Mora, G, Hoppert, M, & Fulda, M. (2008). Mutants of Saccharomyces cerevisiae deficient in acyl-CoA synthetases secrete fatty acids due to interrupted fatty acid recycling. The FEBS Journal, 275(11), 2765–2778.
31. Sherwood, KE, Cano, DJ, & Maupin-Furlow, JA. (2009). Glycerol-mediated repression of glucose metabolism and glycerol kinase as the sole route of glycerol catabolism in the haloarchaeon Haloferax volcanii. Journal of Bacteriology, 191(13), 4307–4315.
32. Sitepu, IR, Garay, LA, Sestric, R, Levin, D, Block, DE, German, JB, & Boundy-Mills, KL. (2014). Oleaginous yeasts for biodiesel: Current and future trends in biology and production. Biotechnology Advances, 32(7), 1336–1360.
33. Sorda, G, Banse, M, & Kemfert, C. (2010). An overview of biofuel policies across the world. Energy Policy, 38(11), 6977–6988.
34. Steen, EJ, Kang, Y, Bokinsky, G, Hu, Z, Schirmer, A, McClure, A, … Keasling, JD. (2010). Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature, 463(7280), 559–562.
35. Waltermann, M, & Steinbuchel, A. (2005). Neutral lipid bodies in prokaryotes: Recent insights into structure, formation, and relationship to eukaryotic lipid depots. Journal of Bacteriology, 187(11), 3607–3619.
36. Wang, W, Wei, H, Knoshaug, E, Van Wychen, S, Xu, Q, Himmel, ME, & Zhang, M. (2016). Fatty alcohol production in Lipomyces starkeyi and Yarrowia lipolytica. Biotechnol Biofuels, 9, 227.
37. Workman, M, Holt, P, & Thykaer, J. (2013). Comparing cellular performance of Yarrowia lipolytica during growth on glucose and glycerol in submerged cultivations. AMB Express, 3(1), 58.
38. Xu, P, Gu, Q, Wang, W, Wong, L, Bower, AG, Collins, CH, & Koffas, MA. (2013). Modular optimization of multi-gene pathways for fatty acids production in E. coli. Nature Communications, 4, 1409.
39. Xu, P, & Koffas, M. (2010). Metabolic engineering of Escherichia coli for biofuel production. Biofuels, 1(3), 493–504.
40. Xu, P, Li, L, Zhang, F, Stephanopoulos, G, & Koffas, M. (2014). Improving fatty acids production by engineering dynamic pathway regulation and metabolic control. Proceedings of the National Academy of Sciences of the United States of America, 111(31), 11299–11304.
41. Xu, P, Qiao, K, Ahn, WS, & Stephanopoulos, G. (2016). Engineering Yarrowia lipolytica as a platform for synthesis of drop-in transportation fuels and oleochemicals. Proceedings of the National Academy of Sciences of the United States of America, 113(39), 10848–10853.
42. Xu, P, Qiao, K, & Stephanopoulos, G. (2017). Engineering oxidative stress defense pathways to build a robust lipid production platform in Yarrowia lipolytica. Biotechnology and Bioengineering, 114(7), 1521–1530.
43. Yarmolinsky, MB, Wiesmeyer, H, Kalckar, HM, & Jordan, E. (1959). Hereditary defects in galactose metabolism in Escherichia coli mutants, II. Galactose-induced sensitivity. Proceeding of the National Academy of Science of the United State of America, 45(12), 1786–1791.
44. Yuzbasheva, EY, Mostova, EB, Andreeva, NI, Yuzbashev, TV, Laptev, IA, Sobolevskaya, TI, & Sineoky, SP. (2017). Co-expression of glucose-6-phosphate dehydrogenase and acyl-CoA binding protein enhances lipid accumulation in the yeast Yarrowia lipolytica. New Biotechnology, 39, 18–21.
45. Yuzbasheva, EY, Yuzbashev, TV, Perkovskaya, NI, Mostova, EB, Vybornaya, TV, Sukhozhenko, AV, … Sineoky, SP. (2015). Cell surface display of Yarrowia lipolytica lipase Lip2p using the cell wall protein YlPir1p, its characterization, and application as a whole-cell biocatalyst. Applied Biochemistry and Biotechnology, 175(8), 3888–3900.
46. Zhang, X, Li, M, Agrawal, A, & San, KY. (2011). Efficient free fatty acid production in Escherichia coli using plant acyl-ACP thioesterases. Metabolic Engineering, 13(6), 713–722.
47. Zweytick D, Athenstaedt K, & Daum G. 2000. Intracellular lipid particles of eukaryotic cells. Biochimica et Biophysica Acta 1469(2):101–20.