Heterologous production of pentane in the oleaginous yeast Yarrowia lipolytica

Journal of Biotechnology

Volumn 165, Issue 3-4, 2013, Pages 184-194

  Blazeck, John ^a   Liu, Leqian ^a   Knight, Rebecca ^b   Alper, Hal S ^a,b  

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

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Alkanes; Metabolic engineering; Pentane; Yarrowia lipolytica

Indexed keywords

BIOSYNTHESIS; CHAINS; ENZYMES; LINOLEIC ACID; METABOLIC ENGINEERING; METABOLISM; PETROLEUM TRANSPORTATION; SUBSTRATES;

HETEROLOGOUS PRODUCTION; METABOLIC PATHWAYS; MICROBIAL PRODUCTION; OLEAGINOUS YEASTS; PENTANE; SOYBEAN LIPOXYGENASE; SUBSTRATE AVAILABILITIES; YARROWIA LIPOLYTICA;

PARAFFINS;

LINOLEIC ACID; LIPOXYGENASE; PENTANE; TRIDECADIENOIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BIOFUEL PRODUCTION; CONTROLLED STUDY; ENZYME SYNTHESIS; FATTY ACID SYNTHESIS; GENE OVEREXPRESSION; HETEROLOGOUS EXPRESSION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SOYBEAN; YARROWIA LIPOLYTICA;

EID: 84877315991     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2013.04.003     Document Type: Article

References (80)

1. Aggelis G., Komaitis M. Enhancement of single cell oil production by Yarrowia lipolytica growing in the presence of Teucrium polium L. aqueous extract. Biotechnology Letters 1999, 21:747-749.
2. Alper H., Fischer C., Nevoigt E., Stephanopoulos G. Tuning genetic control through promoter engineering. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:12678-12683.
3. Andrianarison R.H., Beneytout J.L., Tixier M. An enzymatic conversion of lipoxygenase products by a hydroperoxide lyase in blue-green algae (Oscillatoria sp.). Plant Physiology 1989, 91:1280-1287.
4. Ángel Domínguez E.F., Sánchez M., González F.J., Pérez-Campo F.M., García S., Herrero A.B., San Vicente A., Cabello J., Prado M., Iglesias F.J., Choupina A., Burguillo F.J., Fernández-Lago L., Carmen López M. Non-conventional yeasts as hosts for heterologous protein production. International Microbiology 1998, 1:131-142.
5. Barth G., Gaillardin C. Yarrowia lipolytica. Nonconventional Yeasts in Biotechnology: A Handbook 1996, 313-388. Springer, Heidelberg, Germany. K. Wolf (Ed.).
6. Barth G., Gaillardin C. Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiology Reviews 1997, 19:219-237.
7. Bate N.J., Sivasankar S., Moxon C., Riley J.M.C., Thompson J.E., Rothstein S.J. Molecular characterization of an Arabidopsis gene encoding hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant Physiology 1998, 117:1393-1400.
8. Beopoulos A., Cescut J., Haddouche R., Uribelarrea J.L., Molina-Jouve C., Nicaud J.M. Yarrowia lipolytica as a model for bio-oil production. Progress in Lipid Research 2009, 48:375-387.
9. Beopoulos A., Chardot T., Nicaud J.M. Yarrowia lipolytica: a model and a tool to understand the mechanisms implicated in lipid accumulation. Biochimie 2009, 91:692-696.
10. Beopoulos A., Haddouche R., Kabran P., Dulermo T., Chardot T., Nicaud J.M. 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 2012, 93:1523-1537.
11. Beopoulos A., Mrozova Z., Thevenieau F., Le Dall M.T., Hapala I., Papanikolaou S., Chardot T., Nicaud J.M. Control of lipid accumulation in the yeast Yarrowia lipolytica. Applied and Environmental Microbiology 2008, 74:7779-7789.
12. Beopoulos A., Nicaud J.M., Gaillardin C. An overview of lipid metabolism in yeasts and its impact on biotechnological processes. Applied Microbiology and Biotechnology 2011, 90:1193-1206.
13. Blazeck J., Alper H. Systems metabolic engineering: genome-scale models and beyond. Biotechnology Journal 2010, 5:647-659.
14. Blazeck J., Alper H. Promoter engineering: recent advances in controlling transcription at the most fundamental level. Biotechnology Journal 2012, 8:46-58.
15. Blazeck J., Liu L., Redden H., Alper H. Tuning gene expression in Yarrowia lipolytica by a hybrid promoter approach. Applied and Environmental Microbiology 2011, 77:7905-7914.
16. Blazeck J., Reed B., Garg R., Gerstner R., Pan A., Agarwala V., Alper H. Generalizing a hybrid synthetic promoter approach in Yarrowia lipolytica. Applied Microbiology and Biotechnology 2012, 16:3037-3052.
17. Bourel G., Nicaud J.M., Nthangeni B., Santiago-Gomez P., Belin J.M., Husson F. Fatty acid hydroperoxide lyase of green bell pepper: cloning in Yarrowia lipolytica and biogenesis of volatile aldehydes. Enzyme and Microbial Technology 2004, 35:293-299.
18. Brash A.R. Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. Journal of Biological Chemistry 1999, 274:23679-23682.
19. Cheesbrough T.M., Kolattukudy P.E. Alkane biosynthesis by decarbonylation of aldehydes catalyzed by a particulate preparation from Pisum sativum. Proceedings of the National Academy of Sciences of the United States of America 1984, 81:6613-6617.
20. Chen D.C., Yang B.C., Kuo T.T. One step transformation of yeast in stationary phase. Current Genetics 1992, 21:83-84.
21. Courchesne N.M.D., Parisien A., Wang B., Lan C.Q. Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. Journal of Biotechnology 2009, 141:31-41.
22. Curran K., Alper H. Expanding the chemical palate of cells by combining systems biology and metabolic engineering. Metabolic Engineering 2012, 14:289-297.
23. Davidow L.S., Apostolakos D., Odonnell M.M., Proctor A.R., Ogrydziak D.M., Wing R.A., Stasko I., Dezeeuw J.R. Integrative transformation of the yeast Yarrowia lipolytica. Current Genetics 1985, 10:39-48.
24. Dennis M., Kolattukudy P.E. A cobalt-porphyrin enzyme converts a fatty aldehyde to a hydrocarbon and CO. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:5306-5310.
25. 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.
26. Faroon O., Mandell D., Navarro H. Toxicological profile for JP-4 and JP-7. Registry, Centers for Disease Control and Prevention 1995, 1-150.
27. Fickers P., Le Dall M.T., Gaillardin C., Thonart P., Nicaud J.M. New disruption cassettes for rapid gene disruption and marker rescue in the yeast Yarrowia lipolytica. Journal of Microbiological Methods 2003, 55:727-737.
28. Folch J., Lees M., Stanley G.H.S. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 1957, 226:497-509.
29. Fournier P., Abbas A., Chasles M., Kudla B., Ogrydziak D.M., Yaver D., Xuan J.W., Peito A., Ribet A.M., Feynerol C., He F., Gaillardin C. Colocalization of centromeric and replicative functions on autonomously replicating sequences isolated from the yeast Yarrowia lipolytica. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:4912-4916.
30. Gabaldon T. Peroxisome diversity and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 2010, 365:765-773.
31. Gardner H.W., Weisleder D., Plattner R.D. Hydroperoxide lyase and other hydroperoxide-metabolizing activity in tissues of soybean, Glycine max. Plant Physiology 1991, 97:1059-1072.
32. Garssen G.J., Vliegenthart J.F., Boldingh J. An anaerobic reaction between lipoxygenase, linoleic acid and its hydroperoxides. Biochemical Journal 1971, 122:327-332.
33. Goldstein A.L., McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 1999, 15:1541-1553.
34. Guldener U., Heck S., Fiedler T., Beinhauer J., Hegemann J.H. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Research 1996, 24:2519-2524.
35. Guttikonda S.K., Trupti J., Bisht N.C., Chen H., An Y.Q.C., Pandey S., Xu D., Yu O. Whole genome co-expression analysis of soybean cytochrome P450 genes identifies nodulation-specific P450 monooxygenases. BMC Plant Biology 2010, 10:1-19.
36. Harper C., Liccione J. Toxicological profile for gasoline. Services, Centers for Disease Control and Prevention 1995, 1-224.
37. Hong S., Sharpe P., Xue Z., Yadav N., Zhu Q. Peroxisome Biogenesis Factor Protein (pex) Disruptions for Altering the Content of Polyunsaturated Fatty Acids and the Total Lipid Content in Oleaginous Eukaryotic Organisms 2012, E. I. du Pont de Nemours and Company, Wilmington, DE, USA.
38. IARC IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: Occupational Exposures in Petroleum Refining; Crude Oil and Major Petroleum Fuels 1989, 159-201. World Health Organization, International Agency for Research on Cancer, Lyon, France.
39. Juretzek T., Le Dall M.T., Mauersberger S., Gaillardin C., Barth G., Nicaud J.M. Vectors for gene expression and amplification in the yeast Yarrowia lipolytica. Yeast 2001, 18:97-113.
40. Kamisaka Y., Tomita N., Kimura K., Kainou K., Uemura H. DGA1(diacylglycerol acyltransferase gene) overexpression and leucine biosynthesis significantly increase lipid accumulation in the delta snf2 disruptant of Saccharomyces cerevisiae. Biochemical Journal 2007, 408:61-68.
41. Kirby K.S. A new method for the isolation of ribonucleic acids from mammalian tissues. Biochemical Journal 1956, 64:405-408.
42. Kizer L., Pitera D.J., Pfleger B.F., Keasling J.D. Application of functional genomics to pathway optimization for increased isoprenoid production. Applied and Environmental Microbiology 2008, 74:3229-3241.
43. Ledall M.T., Nicaud J.M., Gaillardin C. Multiple-copy integration in the yeast Yarrowia lipolytica. Current Genetics 1994, 26:38-44.
44. Lu P.-Y. The Installation Restoration Program Toxicology Guide 1989, Wright-Patterson Air Force Base, OH.
45. Madzak C., Gaillardin C., Beckerich J.M. Heterologous protein expression and secretion in the non-conventional yeast Yarrowia lipolytica: a review. Journal of Biotechnology 2004, 109:63-81.
46. 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. Journal of Molecular Microbiology and Biotechnology 2000, 2:207-216.
47. Makri A., Fakas S., Aggelis G. Metabolic activities of biotechnological interest in Yarrowia lipolytica grown on glycerol in repeated batch cultures. Bioresource Technology 2010, 101:2351-2358.
48. Martin V.J.J., Pitera D.J., Withers S.T., Newman J.D., Keasling J.D. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nature Biotechnology 2003, 21:796-802.
49. Matoba T., Hidaka H., Kitamura K., Kaizuma N., Kito M. Contribution of hydroperoxide lyase activity to n-hexanal formation in soybean. Journal of Agricultural and Food Chemistry 1985, 33:856-858.
50. Matsui K., Shibutani M., Hase T., Kajiwara T. Bell pepper fruit fatty acid hydroperoxide lyase is a cytochrome P450 (CYP74B). FEBS Letters 1996, 394:21-24.
51. Matsuoka M., Matsubara M., Daidoh H., Imanaka T., Uchida K., Aiba S. Analysis of regions essential for the function of chromosomal replicator sequences from Yarrowia lipolytica. Molecular & General Genetics 1993, 237:327-333.
52. Minor W., Steczko J., Stec B., Otwinowski Z., Bolin J.T., Walter R., Axelrod B. Crystal structure of soybean lipoxygenase L-l at 1.4 angstrom resolution. Biochemistry 1996, 35:10687-10701.
53. Mlickova K., Roux E., Athenstaedt K., d'Andrea S., Daum G., Chardot T., Nicaud J.M. Lipid accumulation, lipid body formation, and acyl coenzyme A oxidases of the yeast Yarrowia lipolytica. Applied and Environmental Microbiology 2004, 70:3918-3924.
54. 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(11):e27966. 10.1371/journal.pone.0027966.
55. Muller S., Sandal T., Kamp-Hansen P., Dalboge H. Comparison of expression systems in the yeasts Saccharomyces cerevisiae, Hansenula polymorpha, Klyveromyces lactis, Schizosaccharomyces pombe and Yarrowia lipolytica. Cloning of two novel promoters from Yarrowia lipolytica. Yeast 1998, 14:1267-1283.
56. Mumberg D., Muller R., Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995, 156:119-122.
57. Paik M.J., Kim H., Lee J., Brand J., Kim Y.R. Separation of triacylglycerols and free fatty acids in microalgal lipids by solid-phase extraction for separate fatty acid profiling analysis by gas chromatography. Journal of Chromatography A 2009, 1216:5917-5923.
58. 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. European Journal of Lipid Science and Technology 2009, 111:1221-1232.
59. Papanikolaou S., Galiotou-Panayotou M., Chevalot I., Komaitis M., Marc I., Aggelis G. Influence of glucose and saturated free-fatty acid mixtures on citric acid and lipid production by Yarrowia lipolytica. Current Microbiology 2006, 52:134-142.
60. Paradise E.M., Kirby J., Chan R., Keasling J.D. Redirection of flux through the FPP branch-point in Saccharomyces cerevisiae by down-regulating squalene synthase. Biotechnology and Bioengineering 2008, 100:371-378.
61. Pattee H.E., Singleto Ja., Johns E.B. Pentane production by peanut lipoxygenase. Lipids 1974, 9:302-306.
62. Pitera D.J., Newman J.D., Keasling J.D. Optimizing a heterologous mevalonate pathway for the production of terpenoids in Escherichia coli. Abstracts of the General Meeting of the American Society for Microbiology 2004, 104:471.
63. Pitera D.J., Paddon C.J., Newman J.D., Keasling J.D. Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli. Metabolic Engineering 2007, 9:193-207.
64. Porta H., Rocha-Sosa M. Plant lipoxygenases. Physiological and molecular features. Plant Physiology 2002, 130:15-21.
65. Risher J., Bittner P., Rhodes S. Toxicological Profile for JP-5 and JP-8. Registry, Centers for Disease Control and Prevention 1998, 1-200.
66. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 3rd ed.
67. Sanders T.H., Pattee H.E., Singleton J.A. Aerobic pentane production by soybean lipoxygenase isozymes. Lipids 1975, 10:3.
68. Sanders T.H., Pattee H.E., Singleton J.A. Aerobic pentane production by soybean lipoxygenase isozymes. Lipids 1975, 10:568-570.
69. Sanders T.H., Pattee H.E., Singleton J.A. Lipoxygenase isoenzymes of peanut. Lipids 1975, 10:681-685.
70. Savage T.J., Hristova M.K., Croteau R. Evidence for an elongation/reduction/C1-elimination pathway in the biosynthesis of n-heptane in xylem of Jeffrey pine. Plant Physiology 1996, 111:1263-1269.
71. Schirmer A., Rude M.A., Li X.Z., Popova E., del Cardayre S.B. Microbial biosynthesis of alkanes. Science 2010, 329:559-562.
72. Schneiter R., Daum G. Extraction of yeast lipids. Methods in Molecular Biology 2006, 313:41-45.
73. Sherman D., Durrens P., Iragne F., Beyne E., Nikolski M., Souciet J.L. Génolevures complete genomes provide data and tools for comparative genomics of hemiascomycetous yeasts. Nucleic Acids Research 2006, 34:D432-D435.
74. Tabuchi T., Tahara Y., Tanaka M., Yanagiuti S. Preliminary experiments on the mechanism of citrate fermentation in yeasts. Nippon Nogeikagaku Kaishi 1973, 47:617-622.
75. Dulermo T., Nicaud J.M. Involvement of the G3P shuttle and beta-oxidation pathway in the control of TAG synthesis and lipid accumulation in Yarrowia lipolytica. Metabolic Engineering 2011, 13:482-491.
76. Vanheerikhuizen H., Ykema A., Klootwijk J., Gaillardin C., Ballas C., Fournier P. Heterogeneity in the ribosomal RNA genes of the yeast Yarrowia lipolytica - cloning and analysis of two size classes of repeats. Gene 1985, 39:213-222.
77. Vick B.A., Zimmerman D.C. Metabolism of fatty acid hydroperoxides by Chlorella pyrenoidosa. Plant Physiology 1989, 90:125-132.
78. Wang H.J.J., Le Dall M.T., Wache Y., Laroche C., Belin J.M., Gaillardin C., Nicaud J.M. Evaluation of acyl coenzyme A oxidase (Aox) isozyme function in the n-alkane-assimilating yeast Yarrowia lipolytica. Journal of Bacteriology 1999, 181:5140-5148.
79. Watkins J., Krukonis V. Supercritical Fluid Fractionation of JP-8. Aero Propulsion and Power Directorate 1991, Wright Research and Development Center, Air Force Systems Command, Wright-Patterson Air Force Base, OH.
80. Zhu Q., Xue Z., Yadav N., Sharpe P., Fan X., Tyreus B., Short D., Xie D., Boonyaratanakornkit B., Dellomonaco C., Jackson E. Production of omega-3 fatty acids from Yarrowia lipolytica: factors affecting lipid accumulation. SIMB Annual Meeting & Exhibition 2012.