Engineering of unconventional yeast Yarrowia lipolytica for efficient succinic acid production from glycerol at low pH

Metabolic Engineering

Volumn 42, Issue , 2017, Pages 126-133

  Cui, Zhiyong ^a   Gao, Cuijuan ^a,b   Li, Jiaojiao ^a   Hou, Jin ^a   Lin, Carol Sze Ki ^c   Qi, Qingsheng ^a  

^a SHANDONG UNIVERSITY   (China)

^b LINYI UNIVERSITY   (China)

^c CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Acetate: succinate CoA transferase; Acetic acid overflow; Succinic acid production; Yarrowia lipolytica

Indexed keywords

ACETIC ACID; BYPRODUCTS; CARBOXYLATION; GENE ENCODING; GENES; GLYCEROL; ORGANIC ACIDS; PH; PLANTS (BOTANY);

ACETATE: SUCCINATE COA-TRANSFERASE; DECARBOXYLATION REACTIONS; FED-BATCH FERMENTATION; PHOSPHOENOLPYRUVATE CARBOXYKINASE; SUCCINATE DEHYDROGENASE; SUCCINATE PRODUCTION; SUCCINIC ACIDS; YARROWIA LIPOLYTICA;

YEAST;

ACETATE COENZYME A LIGASE; ACETIC ACID; ACETYL COENZYME A; ACETYL COENZYME A HYDROLASE; ACONITATE HYDRATASE; CITRATE SYNTHASE; COENZYME A TRANSFERASE; FUNGAL PROTEIN; GENOMIC DNA; GLYCEROL; GLYOXYLIC ACID; HYDROLASE; ISOCITRATE LYASE; MALATE SYNTHASE; OXOGLUTARATE DEHYDROGENASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PYRUVATE CARBOXYLASE; PYRUVATE DECARBOXYLASE; PYRUVIC ACID; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; SUCCINYL COA SYNTHASE BETA SUBUNIT; SUCCINYL COENZYME A; UNCLASSIFIED DRUG; YLACH PROTEIN; YLACL PROTEIN; YLICL PROTEIN; YLMLS PROTEIN;

ARTICLE; CARBOXYLATION; CELL GROWTH; CITRIC ACID CYCLE; DECARBOXYLATION; ENZYME ACTIVITY; FED BATCH FERMENTATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOMOLOGOUS RECOMBINATION; METABOLIC ENGINEERING; MITOCHONDRION; NONHUMAN; OXIDATION; PH; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; SYNTHESIS; YARROWIA LIPOLYTICA; GENE DELETION; GENETICS; METABOLISM; YARROWIA;

ACETYL COENZYME A; CITRIC ACID CYCLE; COENZYME A-TRANSFERASES; FUNGAL PROTEINS; GENE DELETION; GLYCEROL; HYDROGEN-ION CONCENTRATION; METABOLIC ENGINEERING; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; YARROWIA;

EID: 85020554031     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2017.06.007     Document Type: Article

References (55)

1. Beauprez, J.J., Mey, M.D., Soetaert, W.K., Microbial succinic acid production: natural versus metabolic engineered producers. Process Biochem. 45 (2010), 1103–1114.
2. Bernal, V., Castañocerezo, S., Cánovas, M., Acetate metabolism regulation in Escherichia coli: carbon overflow, pathogenicity, and beyond. Appl. Microbiol. Biotechnol. 100 (2016), 8985–9001.
3. Borges, E.R., Pereira, N., Succinate production from sugarcane bagasse hemicellulose hydrolysate by Actinobacillus succinogenes. J. Ind. Microbiol. 38 (2010), 1001–1011.
4. Cao, Y., Zhang, R., Sun, C., Cheng, T., Liu, Y., Xian, M., Fermentative succinate production: an emerging technology to replace the traditional petrochemical processes. BioMed. Res. Int., 2013, 2013, 723412.
5. Celińska, E., Ledesma-Amaro, R., Larroude, M., Rossignol, T., Pauthenier, C., Nicaud, J.M., Golden Gate Assembly system dedicated to complex pathway manipulation in Yarrowia lipolytica. Microb. Biotechnol., 10, 2017.
6. Chen, D.C., Beckerich, J.M., Gaillardin, C., One-step transformation of the dimorphic yeast Yarrowia lipolytica. Appl. Microbiol. Biotechnol., 48, 1997, 232.
7. Chen, X., Mitochondrial engineering of the TCA cycle for fumarate production. Metab. Eng., 31, 2015, 62.
8. Chen, X., Modular optimization of multi-gene pathways for fumarate production. Metab. Eng. 33 (2016), 76–85.
9. Cok, B., Tsiropoulos, I., Roes, A.L., Patel, M.K., Succinic acid production derived from carbohydrates: an energy and greenhouse gas assessment of a platform chemical toward a bio-based economy. Biofuels Bioprod. Bioref. 8 (2013), 16–29.
10. Fleck, C.B., Brock, M., Re-characterisation of Saccharomyces cerevisiae Ach1p: fungal CoA-transferases are involved in acetic acid detoxification. Fungal Genet. Biol. 46 (2009), 473–485.
11. Gao, C., Yang, X., Wang, H., Rivero, C.P., Chong, L., Cui, Z., Qi, Q., Lin, C.S.K., Robust succinic acid production from crude glycerol using engineered Yarrowia lipolytica. Biotechnol. Biofuels, 9, 2016, 179.
12. Gao, S., Han, L., Zhu, L., Ge, M., Yang, S., Jiang, Y., Chen, D., One-step integration of multiple genes into the oleaginous yeast Yarrowia lipolytica. Biotechnol. Lett. 36 (2014), 2523–2528.
13. Gao, S., Tong, Y., Zhu, L., Ge, M., Zhang, Y., Chen, D., Jiang, Y., Yang, S., Iterative integration of multiple-copy pathway genes in Yarrowia lipolytica for heterologous β-carotene production. Metab. Eng., 2017.
14. Gibson, D.G., Young, L., Chuang, R.Y., Venter, J.C., Smith, H.O., Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods, 6, 2009, 343.
15. Gonçalves, F.A., Colen, G., Takahashi, J.A., Yarrowia lipolytica and its multiple applications in the biotechnological industry. Sci. World J., 2014, 2014, 476207.
16. van Grinsven, K.W., Rosnowsky, S., van Weelden, S.W., Pütz, S., Van, d.G.M., Martin, W., van Hellemond, J.J., Tielens, A.G., Henze, K., Acetate: succinate CoA-transferase in the hydrogenosomes of Trichomonas vaginalis: identification and characterization. J. Biol. Chem. 283 (2008), 1411–1418.
17. Guo, H., Liu, P., Madzak, C., Du, G., Zhou, J., Chen, J., Identification and application of keto acids transporters in Yarrowia lipolytica. Sci. Rep., 5, 2014, 8138.
18. Jansen, M.L., Gulik, W.M.V., Towards large scale fermentative production of succinic acid. Curr. Opin. Biotechnol., 30, 2014, 190.
19. Jost, B., Holz, M., Aurich, A., Barth, G., Bley, T., Müller, R.A., The influence of oxygen limitation for the production of succinic acid with recombinant strains of Yarrowia lipolytica. Appl. Microbiol. Biotechnol. 99 (2015), 1675–1686.
20. Juszczyk, P., Tomaszewska, L., Rymowicz, W., 2013. Production of mannitol by Yarrowia lipolytica in fed-batch fermentation. In: Proceedings of the International Conference on Advances in Biotechnology.
21. Kim, P., Laivenieks, M., Vieille, C., Zeikus, J.G., Effect of overexpression of Actinobacillus succinogenes phosphoenolpyruvate carboxykinase on succinate production in Escherichia coli. Appl. Environ. Microbiol. 70 (2004), 1238–1241.
22. König, S., Subunit structure, function and organisation of pyruvate decarboxylases from various organisms. Biochimica et Biophysica Acta (BBA)-protein. Struct. Mol. Enzymol. 1385 (1998), 271–286.
23. Ledesma-Amaro, R., Nicaud, J.M., Metabolic engineering for expanding the substrate range of Yarrowia lipolytica. Trends Biotechnol., 34, 2016, 798.
24. Lee, P.C., Lee, W.G., Sang, Y.L., Chang, H.N., Chang, Y.K., Fermentative production of succinic acid from glucose and corn steep liquor by Anaerobiospirillum succiniciproducens. Biotechnol. Bioprocess Eng. 5 (2000), 379–381.
25. Li, Y., Li, M., Xu, Z., Peng, Y., Liang, Q., Qi, Q., A novel whole-phase succinate fermentation strategy with high volumetric productivity in engineered Escherichia coli. Bioresour. Technol., 149, 2013, 333.
26. Li, Z.J., Qiao, K., Liu, N., Stephanopoulos, G., Engineering Yarrowia lipolytica for poly-3-hydroxybutyrate production. J. Ind. Microbiol. Biotechnol., 2016, 1–8.
27. Liang, Q., Qi, Q., From a co-production design to an integrated single-cell biorefinery. Biotechnol. Adv., 32, 2014, 1328.
28. Liu, H.H., Ji, X.J., Huang, H., Biotechnological applications of Yarrowia lipolytica: past, present and future. Biotechnol. Adv. 33 (2015), 1522–1546.
29. Liu, L., Alper, H.S., Draft genome sequence of the oleaginous yeast Yarrowia lipolytica PO1f, a commonly used metabolic engineering host. Genome Announc., 2, 2014.
30. Madzak, C., Gaillardin, C., Beckerich, J.M., Heterologous protein expression and secretion in the non-conventional yeast Yarrowia lipolytica: a review. J. Biotechnol. 109 (2004), 63–81.
31. Mckinlay, J.B., Vieille, C., Zeikus, J.G., Prospects for a bio-based succinate industry. Appl. Microbiol. Biotechnol., 76, 2007, 727.
32. Nicaud, J.M., Yarrowia lipolytica. Yeast 29 (2012), 409–418.
33. Raab, A.M., Lang, C., Oxidative versus reductive succinic acid production in the yeast Saccharomyces cerevisiae. Bioeng. Bugs. 2 (2011), 120–123.
34. Raab, A.M., Gebhardt, G., Bolotina, N., Weusterbotz, D., Lang, C., Metabolic engineering of Saccharomyces cerevisiae for the biotechnological production of succinic acid. Metab. Eng. 12 (2010), 518–525.
35. Rezaei, M.N., Aslankoohi, E., Verstrepen, K.J., Courtin, C.M., Contribution of the tricarboxylic acid (TCA) cycle and the glyoxylate shunt in Saccharomyces cerevisiae to succinic acid production during dough fermentation. Int. J. Food Microbiol. 204 (2015), 24–32.
36. Rywin´Ska, A., Juszczyk, P., Wojtatowicz, M., Robak, M., Lazar, Z., Tomaszewska, L., Rymowicz, W., Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass-. Bioenergy 48 (2013), 148–166.
37. Schwartz, C.M., Hussain, M.S., Blenner, M., Wheeldon, I., Synthetic RNA polymerase III promoters facilitate high efficiency CRISPR-Cas9 mediated genome editing in Yarrowia lipolytica. ACS Synth. Biol., 5, 2016, 356.
38. Srere, P.A., Citryl-CoA and the citrate condensing enzyme. Biochim. Et. Biophys. Acta 77 (1963), 693–696.
39. Starai, V.J., Gardner, J.G., Escalantesemerena, J.C., Residue Leu-641 of Acetyl-CoA synthetase is critical for the acetylation of residue Lys-609 by the protein acetyltransferase enzyme of Salmonella enterica. J. Biol. Chem., 280, 2005, 26200.
40. Tan, J.P., Jahim, J.M., Wu, T.Y., Harun, S., Kim, B.H., Mohammad, A.W., Insight into biomass as a renewable carbon source for the production of succinic acid and the factors affecting the metabolic flux toward higher succinate yield. Ind. Eng. Chem. Res. 53 (2014), 16123–16134.
41. Tan, Z., Zhu, X., Chen, J., Li, Q., Zhang, X., Activating phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxykinase in combination for improvement of succinate production. Appl. Environ. Microbiol. 79 (2013), 4838–4844.
42. Tomaszewska, L., Rywin´Ska, A., Gładkowski, W., Production of erythritol and mannitol by Yarrowia lipolytica yeast in media containing glycerol. J. Ind. Microbiol. Biotechnol. 39 (2012), 1333–1343.
43. Vuoristo, K.S., Mars, A.E., Sanders, J.P., Eggink, G., Weusthuis, R.A., Metabolic engineering of TCA cycle for production of chemicals. Trends Biotechnol. 34 (2015), 191–197.
44. 2 deprivation. Biotechnol. Lett. 38 (2016), 1–7.
45. Wang, G.Y., Zhang, Y., Chi, Z., Liu, G.L., Wang, Z.P., Chi, Z.M., Role of pyruvate carboxylase in accumulation of intracellular lipid of the oleaginous yeast Yarrowia lipolytica ACA-DC 50109. Appl. Microbiol. Biotechnol., 99, 2015, 1637.
46. Werpy, T.A., Top value added chemicals from biomass: I. results of screening for potential candidates from sugars and synthesis gas. Synth. Fuels., 2004.
47. Yan, D., Wang, C., Zhou, J., Liu, Y., Yang, M., Xing, J., Construction of reductive pathway in Saccharomyces cerevisiae for effective succinic acid fermentation at low pH value. Bioresour. Technol., 156, 2014, 232.
48. Yin, X., Madzak, C., Du, G., Zhou, J., Chen, J., Enhanced alpha-ketoglutaric acid production in Yarrowia lipolytica WSH-Z06 by regulation of the pyruvate carboxylation pathway. Appl. Microbiol. Biotechnol. 96 (2012), 1527–1537.
49. Yin, X., Li, J., Shin, H.D., Du, G., Liu, L., Chen, J., Metabolic engineering in the biotechnological production of organic acids in the tricarboxylic acid cycle of microorganisms: advances and prospects. Biotechnol. Adv. 33 (2015), 830–841.
50. Yun, C., Ach1 is involved in shuttling mitochondrial acetyl units for cytosolic C2 provision in Saccharomyces cerevisiae lacking pyruvate decarboxylase. FEMS Yeast Res., 15, 2015.
51. Yuzbashev, T.V., Yuzbasheva, E.Y., Sobolevskaya, T.I., Laptev, I.A., Vybornaya, T.V., Larina, A.S., Matsui, K., Fukui, K., Sineoky, S.P., Production of succinic acid at low pH by a recombinant strain of the aerobic yeast Yarrowia lipolytica. Biotechnol. Bioeng. 107 (2010), 673–682.
52. 13C flux analysis of a succinate dehydrogenase deficient strain of Yarrowia lipolytica. Biotechnol. Bioeng. 113 (2016), 2425–2432.
53. Zeikus, J.G., Jain, M.K., Elankovan, P., Biotechnology of succinic acid production and markets for derived industrial products. Appl. Microbiol. Biotechnol. 51 (1999), 545–552.
54. Zhang, F., Li, J., Liu, H., Liang, Q., Qi, Q., ATP-based ratio regulation of glucose and xylose improved succinate production. Plos One, 11, 2016, e0157775.
55. Zhu, Q., Jackson, E.N., Metabolic engineering of Yarrowia lipolytica for industrial applications. Curr. Opin. Biotechnol. 36 (2015), 65–72.