Frontiers of yeast metabolic engineering: Diversifying beyond ethanol and Saccharomyces

Current Opinion in Biotechnology

Volumn 24, Issue 6, 2013, Pages 1023-1030

  Liu, Leqian ^a   Redden, Heidi ^a   Alper, Hal S ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

E. COLI; INDUSTRIAL PRODUCT; MICROBIAL SYSTEM; ORGANIC MOLECULES; POLYKETIDES; SACCHAROMYCES; SUGAR DERIVATIVES; VALUE-ADDED CHEMICALS;

BIODEGRADATION; DERIVATIVES; ESCHERICHIA COLI; ETHANOL; METABOLIC ENGINEERING; ORGANIC CHEMICALS;

YEAST;

ALCOHOL; AROMATIC COMPOUND; CARBOHYDRATE DERIVATIVE; CARBOXYLIC ACID; FAT; FATTY ACID; LIPID; NARINGENIN; POLYKETIDE; RIBOFLAVIN; SUGAR ALCOHOL; TERPENE;

ALCOHOL PRODUCTION; ASHBYA GOSSYPII; BIOENGINEERING; BIOTECHNOLOGICAL PRODUCTION; CANDIDA BOIDINII; CANDIDA FAMATA; CLAVICEPS PURPUREA; FATTY ACID OXIDATION; METABOLIC ENGINEERING; NONHUMAN; PHAFFIA RHODOZYMA; PICHIA PASTORIS; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SCHEFFERSOMYCES STIPITIS; SCHIZOSACCHAROMYCES POMBE; SPATHASPORA PASSALIDARUM; YARROWIA LIPOLYTICA; YEAST;

ESCHERICHIA COLI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

BIOTECHNOLOGY; CARBOHYDRATES; ESCHERICHIA COLI; ETHANOL; LIPIDS; METABOLIC ENGINEERING; POLYKETIDES; SACCHAROMYCES CEREVISIAE; TERPENES; YEASTS;

EID: 84887624541     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2013.03.005     Document Type: Review

References (86)

1. Krivoruchko A., Siewers V., Nielsen J. Opportunities for yeast metabolic engineering: lessons from synthetic biology. Biotechnol J 2011, 6:262-276.
2. Siddiqui M.S., Thodey K., Trenchard I., Smolke C.D. Advancing secondary metabolite biosynthesis in yeast with synthetic biology tools. FEMS Yeast Res 2012, 12:144-170.
3. 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.
4. Peralta-Yahya P.P., Zhang F., del Cardayre S.B., Keasling J.D. Microbial engineering for the production of advanced biofuels. Nature 2012, 488:320-328.
5. Lee J.W., Na D., Park J.M., Lee J., Choi S., Lee S.Y. Systems metabolic engineering of microorganisms for natural and non-natural chemicals. Nat Chem Biol 2012, 8:536-546.
6. Pickens L.B., Tang Y., Chooi Y.H. Metabolic engineering for the production of natural products. Annu Rev Chem Biomol Eng 2011, 2:211-236.
7. Dunlop M. Engineering microbes for tolerance to next-generation biofuels. Biotechnol Biofuels 2011, 4:32.
8. Jeffries T.W. Engineering yeasts for xylose metabolism. Curr Opin Biotechnol 2006, 17:320-326.
9. Sellis D., Callahan B.J., Petrov D.A., Messer P.W. Heterozygote advantage as a natural consequence of adaptation in diploids. Proc Natl Acad Sci USA 2011, 108:20666-20671.
10. Farhi M., Marhevka E., Masci T., Marcos E., Eyal Y., Ovadis M., Abeliovich H., Vainstein A. Harnessing yeast subcellular compartments for the production of plant terpenoids. Metab Eng 2011, 13:474-481.
11. Avalos J.L., Fink G.R., Stephanopoulos G. Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat Biotechnol 2013, advance online publication.
12. Rywińska A., Rymowicz W. High-yield production of citric acid by Yarrowia lipolytica on glycerol in repeated-batch bioreactors. J Ind Microbiol Biotechnol 2010, 37:431-435.
13. Börgel D., van den Berg M., Hüller T., Andrea H., Liebisch G., Boles E., Schorsch C., van der Pol R., Arink A., Boogers I., et al. Metabolic engineering of the non-conventional yeast Pichia ciferrii for production of rare sphingoid bases. Metab Eng 2012, 14:412-426.
14. Nevoigt E. Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2008, 72:379-412.
15. Young E., Lee S.-M., Alper H. Optimizing pentose utilization in yeast: the need for novel tools and approaches. Biotechnol Biofuels 2010, 3:24.
16. Fan L.-H., Zhang Z.-J., Yu X.-Y., Xue Y.-X., Tan T.-W. Self-surface assembly of cellulosomes with two miniscaffoldins on Saccharomyces cerevisiae for cellulosic ethanol production. Proc Natl Acad Sci USA 2012, 109:13260-13265.
17. Ha S.-J., Galazka J.M., Rin Kim S., Choi J.-H., Yang X., Seo J.-H., Louise Glass N., Cate J.H.D., Jin Y.-S. Engineered Saccharomyces cerevisiae capable of simultaneous cellobiose and xylose fermentation. Proc Natl Acad Sci USA 2011, 108:504-509.
18. Agbogbo F., Coward-Kelly G. Cellulosic ethanol production using the naturally occurring xylose-fermenting yeast, Pichia stipitis. Biotechnol Lett 2008, 30:1515-1524.
19. Long T.M., Su Y.-K., Headman J., Higbee A., Willis L.B., Jeffries T.W. Cofermentation of glucose, xylose, and cellobiose by the beetle-associated yeast Spathaspora passalidarum. Appl Environ Microbiol 2012, 78:5492-5500.
20. Steen E.J., Chan R., Prasad N., Myers S., Petzold C.J., Redding A., Ouellet M., Keasling J.D. Metabolic engineering of Saccharomyces cerevisiae for the production of n-butanol. Microb Cell Factories 2008, 7.
21. Chen X., Nielsen K.F., Borodina I., Kielland-Brandt M.C., Karhumaa K. Increased isobutanol production in Saccharomyces cerevisiae by overexpression of genes in valine metabolism. Biotechnol Biofuels 2011, 4:21.
22. Kondo T., Tezuka H., Ishii J., Matsuda F., Ogino C., Kondo A. Genetic engineering to enhance the Ehrlich pathway and alter carbon flux for increased isobutanol production from glucose by Saccharomyces cerevisiae. J Biotechnol 2012, 159:32-37.
23. Brat D., Weber C., Lorenzen W., Bode H., Boles E. Cytosolic re-localization and optimization of valine synthesis and catabolism enables increased isobutanol production with the yeast Saccharomyces cerevisiae. Biotechnol Biofuels 2012, 5:65.
24. Toivari M.H., Ruohonen L., Miasnikov A.N., Richard P., Penttilä M. Metabolic engineering of Saccharomyces cerevisiae for conversion of d-glucose to xylitol and other five-carbon sugars and sugar alcohols. Appl Environ Microbiol 2007, 73:5471-5476.
25. Tomaszewska L., Rywinska A., Gladkowski W. Production of erythritol and mannitol by Yarrowia lipolytica yeast in media containing glycerol. J Ind Microbiol Biotechnol 2012, 39:1333-1343.
26. Dmytruk K.V., Yatsyshyn V.Y., Sybirna N.O., Fedorovych D.V., Sibirny A.A. Metabolic engineering and classic selection of the yeast Candida famata (Candida flareri) for construction of strains with enhanced riboflavin production. Metab Eng 2011, 13:82-88.
27. Park E.Y., Ito Y., Nariyama M., Sugimoto T., Lies D., Kato T. The improvement of riboflavin production in Ashbya gossypii via disparity mutagenesis and DNA microarray analysis. Appl Microbiol Biotechnol 2011, 91:1315-1326.
28. Kamzolova S., Yusupova A., Vinokurova N., Fedotcheva N., Kondrashova M., Finogenova T., Morgunov I. Chemically assisted microbial production of succinic acid by the yeast Yarrowia lipolytica grown on ethanol. Appl Microbiol Biotechnol 2009, 83:1027-1034.
29. Zelle R.M., de Hulster E., van Winden W.A., de Waard P., Dijkema C., Winkler A.A., Geertman J.-M.A., van Dijken J.P., Pronk J.T., van Maris A.J.A. Malic acid production by Saccharomyces cerevisiae: engineering of pyruvate carboxylation, oxaloacetate reduction, and malate export. Appl Environ Microbiol 2008, 74:2766-2777.
30. Osawa F., Fujii T., Nishida T., Tada N., Ohnishi T., Kobayashi O., Komeda T., Yoshida S. Efficient production of l-lactic acid by Crabtree-negative yeast Candida boidinii. Yeast 2009, 26:485-496.
31. 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. Appl Environ Microbiol 2008, 74:7779-7789.
32. 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.
33. Tang X., Feng H., Chen W.N. Metabolic engineering for enhanced fatty acids synthesis in Saccharomyces cerevisiae. Metab Eng 2013, 16:95-102.
34. Holic R., Yazawa H., Kumagai H., Uemura H. Engineered high content of ricinoleic acid in fission yeast Schizosaccharomyces pombe. Appl Microbiol Biotechnol 2012, 95:179-187.
35. Kimura K., Tomita N., Uemura H., Aki T., Ono K., Kamisaka Y. Improvement of stearidonic acid production in oleaginous Saccharomyces cerevisiae. Biosci Biotechnol Biochem 2009, 73:1447-1449.
36. Yazawa H., Iwahashi H., Kamisaka Y., Kimura K., Aki T., Ono K., Uemura H. Heterologous production of dihomo-γ-linolenic acid in Saccharomyces cerevisiae. Appl Environ Microbiol 2007, 73:6965-6971.
37. Athalye S.K., Garcia R.A., Wen Z. Use of biodiesel-derived crude glycerol for producing Eicosapentaenoic Acid (EPA) by the fungus Pythium irregulare. J Agric Food Chem 2009, 57:2739-2744.
38. Tavares S., Grotkjær T., Obsen T., Haslam R.P., Napier J.A., Gunnarsson N. Metabolic engineering of Saccharomyces cerevisiae for production of eicosapentaenoic acid, using a novel δ5-desaturase from Paramecium tetraurelia. Appl Environ Microbiol 2011, 77:1854-1861.
39. Zhang B., Rong C., Chen H., Song Y., Zhang H., Chen W. De novo synthesis of trans-10, cis-12 conjugated linoleic acid in oleaginous yeast Yarrowia Lipolytica. Microb Cell Factories 2012, 11:51.
40. Damude H.G., Zhang H., Farrall L., Ripp K.G., Tomb J.-F., Hollerbach D., Yadav N.S. Identification of bifunctional δ12/ω3 fatty acid desaturases for improving the ratio of ω3 to ω6 fatty acids in microbes and plants. Proc Natl Acad Sci USA 2006, 103:9446-9451.
41. Ageitos J., Vallejo J., Veiga-Crespo P., Villa T. Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol 2011, 90:1219-1227.
42. Shi S., Valle-Rodriguez J., Khoomrung S., Siewers V., Nielsen J. Functional expression and characterization of five wax ester synthases in Saccharomyces cerevisiae and their utility for biodiesel production. Biotechnol Biofuels 2012, 5:7.
43. García E.E., Aguedo M., Gomes N., Choquet A., Belo I., Teixeira J.A., Belin J.-M., Waché Y. Production of 3-hydroxy-γ-decalactone, the precursor of two decenolides with flavouring properties, by the yeast Yarrowia lipolytica. J Mol Catal B Enzym 2009, 57:22-26.
44. Schorsch C., Köhler T., Andrea H., Boles E. High-level production of tetraacetyl phytosphingosine (TAPS) by combined genetic engineering of sphingoid base biosynthesis and L-serine availability in the non-conventional yeast Pichia ciferrii. Metab Eng 2012, 14:172-184.
45. Fischer M.J.C., Meyer S., Claudel P., Bergdoll M., Karst F. Metabolic engineering of monoterpene synthesis in yeast. Biotechnol Bioeng 2011, 108:1883-1892.
46. Rico J., Pardo E., Orejas M. Enhanced production of a plant monoterpene by overexpression of the 3-hydroxy-3-methylglutaryl coenzyme a reductase catalytic domain in Saccharomyces cerevisiae. Appl Environ Microbiol 2010, 76:6449-6454.
47. Hong S.Y., Zurbriggen A.S., Melis A. Isoprene hydrocarbons production upon heterologous transformation of Saccharomyces cerevisiae. J Appl Microbiol 2012, 113:52-65.
48. Ro D.K., Paradise E.M., Ouellet M., Fisher K.J., Newman K.L., Ndungu J.M., Ho K.A., Eachus R.A., Ham T.S., Kirby J., et al. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440:940-943.
49. Shiba Y., Paradise E.M., Kirby J., Ro D.K., Keasling J.D. Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab Eng 2007, 9:160-168.
50. Westfall P.J., Pitera D.J., Lenihan J.R., Eng D., Woolard F.X., Regentin R., Horning T., Tsuruta H., Melis D.J., Owens A., et al. Production of amorphadiene in yeast, and its conversion to dihydroartemisinic acid, precursor to the antimalarial agent artemisinin. Proc Natl Acad Sci USA 2012, 109:111-118.
51. Ignea C., Trikka F., Kourtzelis I., Argiriou A., Kanellis A., Kampranis S., Makris A. Positive genetic interactors of HMG2 identify a new set of genetic perturbations for improving sesquiterpene production in Saccharomyces cerevisiae. Microbial Cell Factories 2012, 11:162.
52. Asadollahi M.A., Maury J., Møller K., Nielsen K.F., Schalk M., Clark A., Nielsen J. Production of plant sesquiterpenes in Saccharomyces cerevisiae: effect of ERG9 repression on sesquiterpene biosynthesis. Biotechnol Bioeng 2008, 99:666-677.
53. Albertsen L., Chen Y., Bach L.S., Rattleff S., Maury J., Brix S., Nielsen J., Mortensen U.H. Diversion of flux toward sesquiterpene production in Saccharomyces cerevisiae by fusion of host and heterologous enzymes. Appl Environ Microbiol 2011, 77:1033-1040.
54. Scalcinati G., Knuf C., Partow S., Chen Y., Maury J., Schalk M., Daviet L., Nielsen J., Siewers V. Dynamic control of gene expression in Saccharomyces cerevisiae engineered for the production of plant sesquitepene α-santalene in a fed-batch mode. Metab Eng 2012, 14:91-103.
55. Chen Y., Daviet L., Schalk M., Siewers V., Nielsen J. Establishing a platform cell factory through engineering of yeast acetyl-CoA metabolism. Metab Eng 2013, 15:48-54.
56. Özaydin B., Burd H., Lee T.S., Keasling J.D. Carotenoid-based phenotypic screen of the yeast deletion collection reveals new genes with roles in isoprenoid production. Metab Eng 2013, 15:174-183.
57. Kirby J., Romanini D.W., Paradise E.M., Keasling J.D. Engineering triterpene production in Saccharomyces cerevisiae-beta-amyrin synthase from Artemisia annua. FEBS J 2008, 275:1852-1859.
58. Madsen K.M., Udatha GDBRK, Semba S., Otero J.M., Koetter P., Nielsen J., Ebizuka Y., Kushiro T., Panagiotou G. Linking genotype and phenotype of Saccharomyces cerevisiae strains reveals metabolic engineering targets and leads to triterpene hyper-producers. PLoS One 2011, 6:e14763.
59. Engels B., Dahm P., Jennewein S. Metabolic engineering of taxadiene biosynthesis in yeast as a first step towards Taxol (Paclitaxel) production. Metab Eng 2008, 10:201-206.
60. Zhou Y.J., Gao W., Rong Q., Jin G., Chu H., Liu W., Yang W., Zhu Z., Li G., Zhu G., et al. Modular pathway engineering of diterpenoid synthases and the mevalonic acid pathway for miltiradiene production. J Am Chem Soc 2012, 134:3234-3241.
61. Lange N., Steinbüchel A. β-Carotene production by Saccharomyces cerevisiae with regard to plasmid stability and culture media. Appl Microbiol Biotechnol 2011, 91:1611-1622.
62. Araya-Garay J.M., Feijoo-Siota L., Rosa-dos-Santos F., Veiga-Crespo P., Villa T.G. Construction of new Pichia pastoris X-33 strains for production of lycopene and beta-carotene. Appl Microbiol Biotechnol 2012, 93:2483-2492.
63. Ukibe K., Hashida K., Yoshida N., Takagi H. Metabolic engineering of Saccharomyces cerevisiae for astaxanthin production and oxidative stress tolerance. Appl Environ Microbiol 2009, 75:7205-7211.
64. Najafi N., Ahmadi A.R., Hosseini R., Golkhoo S. Gamma irradiation as a useful tool for the isolation of astaxanthin-overproducing mutant strains of Phaffia rhodozyma. Can J Microbiol 2011, 57:730-734.
65. Beekwilder J., Wolswinkel R., Jonker H., Hall R., de Vos C.H.R., Bovy A. Production of resveratrol in recombinant microorganisms. Appl Environ Microbiol 2006, 72:5670-5672.
66. Zhang Y., Li S.-Z., Li J., Pan X., Cahoon R.E., Jaworski J.G., Wang X., Jez J.M., Chen F., Yu O. Using unnatural protein fusions to engineer resveratrol biosynthesis in yeast and mammalian cells. J Am Chem Soc 2006, 128:13030-13031.
67. Wang Y., Yu O. Synthetic scaffolds increased resveratrol biosynthesis in engineered yeast cells. J Biotechnol 2012, 157:258-260.
68. Shin S.-Y., Jung S.-M., Kim M.-D., Han N.S., Seo J.-H. Production of resveratrol from tyrosine in metabolically engineered Saccharomyces cerevisiae. Enzyme Microb Technol 2012, 51:211-216.
69. Wang Y., Halls C., Zhang J., Matsuno M., Zhang Y., Yu O. Stepwise increase of resveratrol biosynthesis in yeast Saccharomyces cerevisiae by metabolic engineering. Metab Eng 2011, 13:455-463.
70. Sydor T., Schaffer S., Boles E. Considerable increase in resveratrol production by recombinant industrial yeast strains with use of rich medium. Appl Environ Microbiol 2010, 76:3361-3363.
71. Yan Y., Kohli A., Koffas M.A.G. Biosynthesis of natural flavanones in Saccharomyces cerevisiae. Appl Environ Microbiol 2005, 71:5610-5613.
72. Leonard E., Yan Y., Lim K.H., Koffas M.A.G. Investigation of two distinct flavone synthases for plant-specific flavone biosynthesis in Saccharomyces cerevisiae. Appl Environ Microbiol 2005, 71:8241-8248.
73. Trantas E., Panopoulos N., Ververidis F. Metabolic engineering of the complete pathway leading to heterologous biosynthesis of various flavonoids and stilbenoids in Saccharomyces cerevisiae. Metab Eng 2009, 11:355-366.
74. Hansen E.H., Moller B.L., Kock G.R., Bunner C.M., Kristensen C., Jensen O.R., Okkels F.T., Olsen C.E., Motawia M.S., Hansen J. De novo biosynthesis of vanillin in fission yeast (Schizosaccharomyces pombe) and Baker's Yeast (Saccharomyces cerevisiae). Appl Environ Microbiol 2009, 75:2765-2774.
75. Brochado A., Matos C., Moller B., Hansen J., Mortensen U., Patil K. Improved vanillin production in baker's yeast through in silico design. Microbial Cell Factories 2010, 9:84.
76. Curran K.A., Leavitt J.M., Karim A.S., Alper H.S. Metabolic engineering of muconic acid production in Saccharomyces cerevisiae. Metab Eng 2013, 15:55-66.
77. Shao Z., Luo Y., Zhao H. Rapid characterization and engineering of natural product biosynthetic pathways via DNA assembler. Mol Biosyst 2011, 7:1056-1059.
78. Fisch K.M., Bakeer W., Yakasai A.A., Song Z., Pedrick J., Wasil Z., Bailey A.M., Lazarus C.M., Simpson T.J., Cox R.J. Rational domain swaps decipher programming in fungal highly reducing polyketide synthases and resurrect an extinct metabolite. J Am Chem Soc 2011, 133:16635-16641.
79. Askenazi M., Driggers E.M., Holtzman D.A., Norman T.C., Iverson S., Zimmer D.P., Boers M.E., Blomquist P.R., Martinez E.J., Monreal A.W., et al. Integrating transcriptional and metabolite profiles to direct the engineering of lovastatin-producing fungal strains. Nat Biotechnol 2003, 21:150-156.
80. Ng C.Y., Jung M.-Y., Lee J., Oh M.-K. Production of 2,3-butanediol in Saccharomyces cerevisiae by in silico aided metabolic engineering. Microb Cell Factories 2012, 11:68.
81. Mikkelsen M.D., Buron L.D., Salomonsen B., Olsen C.E., Hansen B.G., Mortensen U.H., Halkier B.A. Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform. Metab Eng 2012, 14:104-111.
82. Hawkins K.M., Smolke C.D. Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol 2008, 4:564-573.
83. Veiga T., Gombert A.K., Landes N., Verhoeven M.D., Kiel J.A.K.W., Krikken A.M., Nijland J.G., Touw H., Luttik M.A.H., van der Toorn J.C., et al. Metabolic engineering of β-oxidation in Penicillium chrysogenum for improved semi-synthetic cephalosporin biosynthesis. Metab Eng 2012, 14:437-448.
84. Gidijala L., Kiel J.A.K.W., Douma R.D., Seifar R.M., van Gulik W.M., Bovenberg R.A.L., Veenhuis M., van der Klei I.J. An engineered yeast efficiently secreting penicillin. PLoS One 2009, 4.
85. Bayer T.S., Widmaier D.M., Temme K., Mirsky E.A., Santi D.V., Voigt C.A. Synthesis of methyl halides from biomass using engineered microbes. J Am Chem Soc 2009, 131:6508-6515.
86. Lanza A.M., Crook N.C., Alper H.S. Innovation at the intersection of synthetic and systems biology. Curr Opin Biotechnol 2012, 23:712-717.