An evolutionary metabolic engineering approach for enhancing lipogenesis in Yarrowia lipolytica

Metabolic Engineering

Volumn 29, Issue , 2015, Pages 36-45

  Liu, Leqian ^a   Pan, Anny ^a   Spofford, Caitlin ^a   Zhou, Nijia ^a   Alper, Hal S ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Evolutionary metabolic engineering; Lipogenesis; Whole genome sequencing; Yarrowia lipolytica

Indexed keywords

AMINO ACIDS; CELL ENGINEERING; GENES; METABOLISM; PRODUCTIVITY; STRAIN;

BIOMASS GENERATION; GAMMA-AMINOBUTYRIC ACIDS; LIPOGENESIS; METABOLIC ENGINEERING APPROACH; SEMIALDEHYDE DEHYDROGENASE; SPECIFIC PRODUCTIVITY; WHOLE GENOME SEQUENCING; YARROWIA LIPOLYTICA;

METABOLIC ENGINEERING;

YARROWIA LIPOLYTICA;

FUNGAL PROTEIN; LIPID; SUCCINATE SEMIALDEHYDE DEHYDROGENASE;

BIOSYNTHESIS; DIRECTED MOLECULAR EVOLUTION; GENETICS; LIPOGENESIS; METABOLIC ENGINEERING; METABOLISM; YARROWIA;

DIRECTED MOLECULAR EVOLUTION; FUNGAL PROTEINS; LIPIDS; LIPOGENESIS; METABOLIC ENGINEERING; SUCCINATE-SEMIALDEHYDE DEHYDROGENASE; YARROWIA;

EID: 84924176808     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2015.02.003     Document Type: Article

References (62)

1. Abatemarco J., Hill A., Alper H.S. Expanding the metabolic engineering toolbox with directed evolution. Biotechnol. J. 2013, 8:1397-1410.
2. Bach B., Meudec E., Lepoutre J.-P., Rossignol T., Blondin B., Dequin S., Camarasa C. New insights into γ-aminobutyric acid catabolism: evidence for γ-hydroxybutyric acid and polyhydroxybutyrate synthesis in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2009, 75:4231-4239.
3. Beller H.R., Goh E.-B., Keasling J.D. Genes involved in long-chain alkene biosynthesis in Micrococcus luteus. Appl. Environ. Microbiol. 2010, 76:1212-1223.
4. Beopoulos A., Cescut J., Haddouche R., Uribelarrea J.-L., Molina-Jouve C., Nicaud J.-M. Yarrowia lipolytica as a model for bio-oil production. Prog. Lipid Res. 2009, 48:375-387.
5. Blazeck J., Hill A., Liu L., Knight R., Miller J., Pan A., Otoupal P., Alper H.S. Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production. Nat. Commun. 2014, 5. (Article number 3131), 10.1038/ncomms4131.
6. Blazeck J., Liu L., Knight R., Alper H.S. Heterologous production of pentane in the oleaginous yeast Yarrowia lipolytica. J. Biotechnol. 2013, 165:184-194.
7. Blazeck J., Liu L., Redden H., Alper H. Tuning gene expression in Yarrowia lipolytica by a hybrid promoter approach. Appl. Environ. Microbiol. 2011, 77:7905-7914.
8. Cao J., Barbosa J.M., Singh N.K., Locy R.D. GABA shunt mediates thermotolerance in Saccharomyces cerevisiae by reducing reactive oxygen production. Yeast 2013, 30:129-144.
9. Cardenas M.E., Cutler N.S., Lorenz M.C., Di Como C.J., Heitman J. The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 1999, 13:3271-3279.
10. Cingolani, P., Patel, V.M., Coon, M., Nguyen, T., Land, S.J., Ruden, D.M. Lu, X., 2012. Using Drosophila melanogaster as a model for genotoxic chemical mutational studies with a new program, SnpSift. Front. Gene. 3:35, . http://dx.doi.org/10.3389/fgene.2012.00035.
11. Clark G.J., Bushell M.E. Oxygen limitation can induce microbial secondary metabolite formation: investigations with miniature electrodes in shaker and bioreactor culture. Microbiology 1995, 141:663-669.
12. Coleman S.T., Fang T.K., Rovinsky S.A., Turano F.J., Moye-Rowley W.S. Expression of a glutamate decarboxylase homolog is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J. Biol. Chem. 2001, 276:244-250.
13. Curran K.A., Alper H.S. Expanding the chemical palate of cells by combining systems biology and metabolic engineering. Metab. Eng. 2012, 14:289-297.
14. Dujon B., Sherman D., Fischer G., Durrens P., Casaregola S., Lafontaine I., de Montigny J., Marck C., Neuveglise C., Talla E., Goffard N., Frangeul L., Aigle M., Anthouard V., Babour A., Barbe V., Barnay S., Blanchin S., Beckerich J.-M., Beyne E., Bleykasten C., Boisrame A., Boyer J., Cattolico L., Confanioleri F., de Daruvar A., Despons L., Fabre E., Fairhead C., Ferry-Dumazet H., Groppi A., Hantraye F., Hennequin C., Jauniaux N., Joyet P., Kachouri R., Kerrest A., Koszul R., Lemaire M., Lesur I., Ma L., Muller H., Nicaud J.-M., Nikolski M., Oztas S., Ozier-Kalogeropoulos O., Pellenz S., Potier S., Richard G.-F., Straub M.-L., Suleau A., Swennen D., Tekaia F., Wesolowski-Louvel M., Westhof E., Wirth B., Zeniou-Meyer M., Zivanovic I., Bolotin-Fukuhara M., Thierry A., Bouchier C., Caudron B., Scarpelli C., Gaillardin C., Weissenbach J., Wincker P., Souciet J.-L. Genome evolution in yeasts. Nature 2004, 430:35-44.
15. Evans C.T., Ratledge C. Effect of nitrogen source on lipid accumulation in oleaginous yeasts. J. Gen. Microbiol. 1984, 130:1693-1704.
16. Fendt S.-M., Bell E.L., Keibler M.A., Olenchock B.A., Mayers J.R., Wasylenko T.M., Vokes N.I., Guarente L., Heiden M.G.V., Stephanopoulos G. Reductive glutamine metabolism is a function of the α-ketoglutarate to citrate ratio in cells. Nat. Commun. 2013, 4. (Article number 2236), 10.1038/ncomms3236.
17. Folch J., Lees M., Stanley G.H.S. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
18. Fong S.S., Burgard A.P., Herring C.D., Knight E.M., Blattner F.R., Maranas C.D., Palsson B.O. In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnol. Bioeng. 2005, 91:643-648.
19. Gaillardin C., Ribet A.M., Heslot H. Integrative transformation of the yeast Yarrowia lipolytica. Curr. Genet. 1985, 10:49-58.
20. Gebre S., Connor R., Xia Y., Jawed S., Bush J.M., Bard M., Elsalloukh H., Tang F. Osh6 overexpression extends the lifespan of yeast by increasing vacuole fusion. Cell Cycle 2012, 11:2176-2188.
21. Greenspan P., Mayer E.P., Fowler S.D. Nile red: a selective fluroscent stain for intracelluluar lipid droplets. J. Cell Biol. 1985, 100:965-973.
22. Guo D., Zhu J., Deng Z., Liu T. Metabolic engineering of Escherichia coli for production of fatty acid short-chain esters through combination of the fatty acid and 2-keto acid pathways. Metab. Eng. 2014, 22:69-75.
23. Hamilton M.L., Haslam R.P., Napier J.A., Sayanova O. Metabolic engineering of Phaeodactylum tricornutum for the enhanced accumulation of omega-3 long chain polyunsaturated fatty acids. Metab. Eng. 2014, 22:3-9.
24. Hong K.-K., Nielsen J. Recovery of phenotypes obtained by adaptive evolution through inverse metabolic engineering. Appl. Environ. Microbiol. 2012, 78:7579-7586.
25. Jiang L.-Y., Chen S.-G., Zhang Y.-Y., Liu J.-Z. Metabolic evolution of Corynebacterium glutamicum for increased production of l-ornithine. BMC Biotechnol. 2013, 13:47.
26. Kamei Y., Tamura T., Yoshida R., Ohta S., Fukusaki E., Mukai Y. GABA metabolism pathway genes, UGA1 and GAD1, regulate replicative lifespan in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 2011, 407:185-190.
27. Kamisaka Y., Noda N., Tomita N., Kimura K., Kodaki T., Hosaka K. Identification of genes affecting lipid content using transposon mutagenesis in Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 2006, 70:646-653.
28. Keasling J.D. Manufacturing molecules through metabolic engineering. Sci. 2010, 330:1355-1358.
29. Le Dall M.-T., Nicaud J.-M., Gaillardin C. Multiple-copy integration in the yeast Yarrowia lipolytica. Curr. Genet. 1994, 26:38-44.
30. Lennen R.M., Pfleger B.F. Microbial production of fatty acid-derived fuels and chemicals. Curr. Opin. Biotechnol. 2013, 24:1044-1053.
31. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
32. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R., Subgroup G.P.D.P The sequence alignment/map format and samtools. Bioinformatics 2009, 25:2078-2079.
33. Liu L., Alper H.S. Draft genome sequence of the oleaginous yeast Yarrowia lipolytica PO1f, a commonly used metabolic engineering host. Genome Announc. 2014, 2(4). e00652-14, 10.1128/genomeA.00652-14.
34. Liu L., Redden H., Alper H.S. Frontiers of yeast metabolic engineering: diversifying beyond ethanol and Saccharomyces. Curr. Opin. Biotechnol. 2013, 24:1023-1030.
35. Liu Q., Guo Y., Li J., Long J., Zhang B., Shyr Y. Steps to ensure accuracy in genotype and SNP calling from Illumina sequencing data. BMC Genomics 2012, 13:S8.
36. Liu Y., Wang C., Yan J., Zhang W., Guan W., Lu X., Li S. Hydrogen peroxide-independent production of alpha-alkenes by OleTJE P450 fatty acid decarboxylase. Biotechnol. Biofuels 2014, 7:28.
37. Madzak C., Treton B., Blanchin-Roland S. Strong hybrid promoters and integrative expression/secretion vectors for quasi-constitutive expression of heterologous proteins in the yeast Yarrowia lipolytica. J. Mol. Microbiol. Biotechnol. 2000, 2:207-216.
38. Matsumoto K.i., Tobitani K., Aoki S., Song Y., Ooi T., Taguchi S. Improved production of poly(lactic acid)-like polyester based on metabolite analysis to address the rate-limiting step. AMB Express 2014, 4:83.
39. Nevoigt E. Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2008, 72:379-412.
40. Papanikolaou S., Chatzifragkou A., Fakas S., Galiotou-Panayotou M., Komaitis M., Nicaud J.-M., Aggelis G. Biosynthesis of lipids and organic acids by Yarrowia lipolytica strains cultivated on glucose. Eur. J. Lipid Sci. Technol. 2009, 111:1221-1232.
41. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
42. Ramos F., El Guezzar M., Grenson M., Wiame J.-M. Mutations affecting the enzymes involved in the utilization of 4-aminobutyric acid as nitrogen source by the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 1985, 149:401-404.
43. Robinson J.T., Thorvaldsdottir H., Winckler W., Guttman M., Lander E.S., Getz G., Mesirov J.P. Integrative genomics viewer. Nat. Biotechnol. 2011, 29:24-26.
44. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5:725-738.
45. Sambrook J. Molecular Cloning: A Laboratory Manual 2000, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. D.W. Russell (Ed.).
46. Santos C.N.S., Xiao W., Stephanopoulos G. Rational, combinatorial, and genomic approaches for engineering l-tyrosine production in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A 2012, 109:13538-13543.
47. Scalcinati G., Otero J.M., Van Vleet J.R.H., Jeffries T.W., Olsson L., Nielsen J. Evolutionary engineering of Saccharomyces cerevisiae for efficient aerobic xylose consumption. FEMS Yeast Res. 2012, 12:582-597.
48. Schirmer A., Rude M.A., Li X., Popova E., del Cardayre S.B. Microbial biosynthesis of alkanes. Science 2010, 329:559-562.
49. Schneiter R., Daum G. Extraction of yeast lipids. Yeast Protocol 2006, vol. 313:41-45. Humana Press.
50. Shiwa Y., Fukushima-Tanaka S., Kasahara K., Horiuchi T., Yoshikawa H. Whole-genome profiling of a novel mutagenesis technique using proofreading-deficient dna polymerase delta. Int. J. Evol. Biol. 2012, 2012:860797.
51. Smith K.M., Liao J.C. An evolutionary strategy for isobutanol production strain development in Escherichia coli. Metab. Eng. 2011, 13:674-681.
52. Staschke K.A., Dey S., Zaborske J.M., Palam L.R., McClintick J.N., Pan T., Edenberg H.J., Wek R.C. Integration of general amino acid control and target of rapamycin (TOR) regulatory pathways in nitrogen assimilation in yeast. J. Biol. Chem. 2010, 285:16893-16911.
53. Steen E.J., Kang Y., Bokinsky G., Hu Z., Schirmer A., McClure A., del Cardayre S.B., Keasling J.D. Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 2010, 463:559-562.
54. Tai M., Stephanopoulos G. Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab. Eng. 2013, 15:1-9.
55. Tapia V E., Anschau A., Coradini A.L., T Franco T., Deckmann A. Optimization of lipid production by the oleaginous yeast Lipomyces starkeyi by random mutagenesis coupled to cerulenin screening. AMB Express 2012, 2:64.
56. Trentacoste E.M., Shrestha R.P., Smith S.R., Glé C., Hartmann A.C., Hildebrand M., Gerwick W.H. Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth. Proc. Natl. Acad. Sci. U.S.A 2013, 110:19748-19753.
57. Winston, F., 2008. EMS and UV Mutagenesis in Yeast. Current Protocols in Molecular Biology. 82:I:13.3B:13.3B.1-13.3B.5.
58. Xue Z., Sharpe P.L., Hong S.-P., Yadav N.S., Xie D., Short D.R., Damude H.G., Rupert R.A., Seip J.E., Wang J., Pollak D.W., Bostick M.W., Bosak M.D., Macool D.J., Hollerbach D.H., Zhang H., Arcilla D.M., Bledsoe S.A., Croker K., McCord E.F., Tyreus B.D., Jackson E.N., Zhu Q. Production of omega-3 eicosapentaenoic acid by metabolic engineering of Yarrowia lipolytica. Nat. Biotechnol. 2013, 31:734-740.
59. Yamane T., Sakai H., Nagahama K., Ogawa T., Matsuoka M. Dissection of centromeric DNA from yeast Yarrowia lipolytica and identification of protein-binding site required for plasmid transmission. J. Biosci. Bioeng. 2008, 105:571-578.
60. Yuan Z., Yin B., Wei D., Yuan Y.A. Structural basis for cofactor and substrate selection by cyanobacterium succinic semialdehyde dehydrogenase. J. Struct. Biol. 2013, 182:125-135.
61. 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. 2012, 14:653-660.
62. Zhu X., Tan Z., Xu H., Chen J., Tang J., Zhang X. Metabolic evolution of two reducing equivalent-conserving pathways for high-yield succinate production in Escherichia coli. Metab. Eng. 2014, 24:87-96.