Surveying the lipogenesis landscape in Yarrowia lipolytica through understanding the function of a Mga2p regulatory protein mutant

Metabolic Engineering

Volumn 31, Issue , 2015, Pages 102-111

  Liu, Leqian ^a   Markham, Kelly ^a   Blazeck, John ^a   Zhou, Nijia ^a   Leon, Dacia ^a   Otoupal, Peter ^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

Lipogenesis; Metabolic engineering; Mga2; Yarrowia; Yeast

Indexed keywords

FATTY ACIDS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES; METABOLISM; PROTEINS; UNSATURATED FATTY ACIDS; YEAST;

COMPARATIVE GENOMICS; ENGINEERED STRAINS; LIPOGENESIS; MGA2; REGULATORY ELEMENTS; REGULATORY PROTEIN; YARROWIA; YARROWIA LIPOLYTICA;

METABOLIC ENGINEERING;

FUNGAL PROTEIN; MUTANT PROTEIN; PROTEIN MGA2P; REGULATOR PROTEIN; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; ACYL COENZYME A DESATURASE; TRANSCRIPTOME;

ARTICLE; CATABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; GLYCOLYSIS; LIPOGENESIS; METABOLIC ENGINEERING; MGA2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; TRANSCRIPTOMICS; YARROWIA LIPOLYTICA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; YARROWIA;

YARROWIA; YARROWIA LIPOLYTICA;

FATTY ACID DESATURASES; FATTY ACIDS, UNSATURATED; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LIPOGENESIS; METABOLIC ENGINEERING; MUTANT PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; TRANSCRIPTOME; YARROWIA;

EID: 84938932084     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2015.07.004     Document Type: Article

References (72)

1. Alper H., Miyaoku K., Stephanopoulos G. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat. Biotechnol. 2005, 23:612-616.
2. Alper H., Moxley J., Nevoigt E., Fink G.R., Stephanopoulos G. Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 2006, 314:1565-1568.
3. Alper H., Stephanopoulos G. Uncovering the gene knockout landscape for improved lycopene production in E. coli. Appl. Microbiol. Biotechnol. 2008, 78:801-810.
4. Andrews, S., 2010. FastQC a Quality-Control Tool for High-throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
5. Athenstaedt K. YALI0E32769g (DGA1) and YALI0E16797g (LRO1) encode major triacylglycerol synthases of the oleaginous yeast Yarrowia lipolytica. Biochim. Biophys. Acta (BBA)-Mol. Cell Biol. Lipids 2011, 1811:587-596.
6. Auld K.L., Brown C.R., Casolari J.M., Komili S., Silver P.A. Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates. Mol. Cell. 2006, 21:861-871.
7. 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.
8. Beopoulos A., Verbeke J., Bordes F., Guicherd M., Bressy M., Marty A., Nicaud J.-M. Metabolic engineering for ricinoleic acid production in the oleaginous yeast Yarrowia lipolytica. Appl. Microbiol. Biotechnol. 2014, 98:251-262.
9. 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, 5:3131.
10. 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.
11. 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.
12. Bricker D.K., Taylor E.B., Schell J.C., Orsak T., Boutron A., Chen Y.C., Cox J.E., Cardon C.M., Van Vranken J.G., Dephoure N., Redin C., Boudina S., Gygi S.P., Brivet M., Thummel C.S., Rutter J. A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 2012, 337:96-100.
13. Chellappa R., Kandasamy P., Oh C.-S., Jiang Y., Vemula M., Martin C.E. The membrane proteins, Spt23p and Mga2p, play distinct roles in the activation of Saccharomyces cerevisiae OLE1 gene expression: fatty acid-mediated regulation of Mga2p activity is independent of its proteolytic processing into a soluble transcription activator. J. Biol. Chem. 2001, 276:43548-43556.
14. Ching T.H. Bioconversion of Unsaturated Fatty Acids to Value-added Products. Applied Biocatalysis in Specialty Chemicals and Pharmaceuticals 2001, 776:92-102. American Chemical Society.
15. 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.
16. 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.
17. Dulermo T., Nicaud J.-M. Involvement of the G3P shuttle and β-oxidation pathway in the control of TAG synthesis and lipid accumulation in Yarrowia lipolytica. Metab. Eng.. 2011, 13:482-491.
18. 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.
19. 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.
20. 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.
21. 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.
22. Hoppe T., Matuschewski K., Rape M., Schlenker S., Ulrich H.D., Jentsch S. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 2000, 102:577-586.
23. Huang D.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Prot. 2008, 4:44-57.
24. Hulsen T., de Vlieg J., Alkema W. BioVenn-a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 2008, 9:488.
25. Jiang Y., Vasconcelles M.J., Wretzel S., Light A., Martin C.E., Goldberg M.A. MGA2 is involved in the low-oxygen response element-dependent hypoxic induction of genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 2001, 21:6161-6169.
26. Kaliszewski, P., Szkopińska, A., Ferreira, T., Świezewska, E., Berges, T., Zoładek, T., 2008. Rsp5p ubiquitin ligase and the transcriptional activators Spt23p and Mga2p are involved in co-regulation of biosynthesis of end products of the mevalonate pathway and triacylglycerol in yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta (BBA)-Mol. Cell Biol. Lipids. 1781, 627-634.
27. Kandasamy P., Vemula M., Oh C.-S., Chellappa R., Martin C.E. Regulation of unsaturated fatty acid biosynthesis in Saccharomyces: the endoplasmic reticulum membrane protein, Mga2p, a transcription activator of the OLE1 gene, regulates the stability of the OLE1 mRNA through exosome-mediated mechanisms. J. Biol. Chem. 2004, 279:36586-36592.
28. Kanehisa M., Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000, 28:27-30.
29. Kaplan R.S., Mayor J.A., Gremse D.A., Wood D.O. High level expression and characterization of the mitochondrial citrate transport protein from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 1995, 270:4108-4114.
30. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
31. Le Dall M.-T., Nicaud J.-M., Gaillardin C. Multiple-copy integration in the yeast Yarrowia lipolytica. Curr. Genet. 1994, 26:38-44.
32. Letunic I., Doerks T., Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 2012, 40:D302-D305.
33. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
34. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R., Genome Project Data Processing S. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
35. Listenberger L.L., Han X., Lewis S.E., Cases S., Farese R.V., Ory D.S., Schaffer J.E. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. 2003, 100:3077-3082.
36. Liu L., Alper H.S. Draft genome sequence of the oleaginous yeast Yarrowia lipolytica PO1f, a commonly used metabolic engineering host. Genome Announcements 2014, 2(4):e00652-14.
37. Liu L., Otoupal P., Pan A., Alper H.S. Increasing expression level and copy number of a Yarrowia lipolytica plasmid through regulated centromere function. FEMS Yeast Res. 2014, 14:1124-1127.
38. Liu L., Pan A., Spofford C., Zhou N., Alper H. An evolutionary metabolic engineering approach for enhancing lipogenesis in Yarrowia lipolytica. Metab. Eng. 2015, 29:36-45.
39. Liu L., Redden H., Alper H.S. Frontiers of yeast metabolic engineering: diversifying beyond ethanol and Saccharomyces. Curr. Opin. Biotechnol. 2013, 24:1023-1030.
40. 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.
41. 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.
42. Micolonghi C., Ottaviano D., Di Silvio E., Damato G., Heipieper H.J., Bianchi M.M. A dual signalling pathway for the hypoxic expression of lipid genes, dependent on the glucose sensor Rag4, is revealed by the analysis of the KlMGA2 gene in Kluyveromyces lactis. Microbiology. 2012, 158:1734-1744.
43. Morin N., Cescut J., Beopoulos A., Lelandais G., Le Berre V., Uribelarrea J.L., Molina-Jouve C., Nicaud J.M. Transcriptomic analyses during the transition from biomass production to lipid accumulation in the oleaginous yeast Yarrowia lipolytica. PLoS One 2011, 6:e27966.
44. Nguyen L.N., Nosanchuk J.D. Lipid droplet formation protects against gluco/lipotoxicity in Candida parapsilosis: an essential role of fatty acid desaturase Ole1. Cell Cycle. 2011, 10:3159-3167.
45. Nicaud J.-M. Yarrowia lipolytica. Yeast 2012, 29:409-418.
46. Oliveros, J.C., 2007. VENNY. An Interactive Tool for Comparing Lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html.
47. Pablo C., Viral M.P., Melissa C., Tung N., Susan J.L., Douglas M.R., Xiangyi L. Using Drosophila melanogaster as a model for genotoxic chemical mutational studies with a new program, SnpSift. Front. Genet. 2012, 3.
48. Paul D., Magbanua Z., Arick M., French T., Bridges S.M., Burgess S.C., Lawrence M.L. Genome sequence of the oleaginous yeast Rhodotorula glutinis ATCC 204091. Genome Announcements 2014, 2.
49. Piwko W., Jentsch S. Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site. Nat. Struct. Mol. Biol. 2006, 13:691-697.
50. 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.. 2015, 29:56-65.
51. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
52. 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.
53. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
54. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press.
55. Schirmer A., Rude M.A., Li X., Popova E., del Cardayre S.B. Microbial biosynthesis of alkanes. Science 2010, 329:559-562.
56. Schneiter R., Daum G. Extraction of yeast lipids. Yeast Protocol 2006, 313:41-45. Humana Press.
57. Seip J., Jackson R., He H., Zhu Q., Hong S.-P. Snf1 is a regulator of lipid accumulation in Yarrowia lipolytica. Appl. Environ. Microbiol. 2013, 79:7360-7370.
58. Shi X., Li J., Zou X., Greggain J., Rødkær S.V., Færgeman N.J., Liang B., Watts J.L. Regulation of lipid droplet size and phospholipid composition by stearoyl-CoA desaturase. J. Lipid Res. 2013, 54:2504-2514.
59. 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.
60. Stephanopoulos, G., Abidi, S.H.I., Microbial Engineering for the Production of Fatty Acids and Fatty Acid Derivatives. Patent, US8765404 B2. 2014.
61. Swaney D.L., Beltrao P., Starita L., Guo A., Rush J., Fields S., Krogan N.J., Villen J. Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat. Method 2013, 10:676-682.
62. 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.
63. Tai, M., Metabolic Engineering of Oleaginous Yeast for the Production of Biofuels. Massachusetts Institute of Technology, 2012, pp. 220 p.
64. Tehlivets O., Scheuringer K., Kohlwein S.D. Fatty acid synthesis and elongation in yeast. Biochim. Biophys. Acta (BBA)-Mol. Cell Biol. Lipids 2007, 1771:255-270.
65. Trapnell C., Roberts A., Goff L., Pertea G., Kim D., Kelley D.R., Pimentel H., Salzberg S.L., Rinn J.L., Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Prot. 2012, 7:562-578.
66. Wang Z.-P., Xu H.-M., Wang G.-Y., Chi Z., Chi Z.-M. Disruption of the MIG1 gene enhances lipid biosynthesis in the oleaginous yeast Yarrowia lipolytica ACA-DC 50109. Biochim. Biophys. Acta (BBA)-Mol. Cell Biol. Lipids 2013, 1831:675-682.
67. Wasylenko T.M., Ahn W.S., Stephanopoulos G. The oxidative pentose phosphate pathway is the primary source of NADPH for lipid overproduction from glucose in Yarrowia lipolytica. Metab. Eng. 2015, 30:27-39.
68. 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.
69. Zhang B., Chen H., Li M., Gu Z., Song Y., Ratledge C., Chen Y., Zhang H., Chen W. Genetic engineering of Yarrowia lipolytica for enhanced production of trans-10, cis-12 conjugated linoleic acid. Microbial Cell Factories. 2013, 12:70.
70. Zhang S., Burkett T.J., Yamashita I., Garfinkel D.J. Genetic redundancy between SPT23 and MGA2: regulators of Ty-induced mutations and Ty1 transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 1997, 17:4718-4729.
71. Zhang S., Skalsky Y., Garfinkel D.J. MGA2 or SPT23 is required for transcription of the δ9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae. Genetics 1999, 151:473-483.
72. Zhu Z., Zhang S., Liu H., Shen H., Lin X., Yang F., Zhou Y.J., Jin G., Ye M., Zou H., Zhao Z.K. A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat. Commun. 2012, 3:1112.