Advances in the metabolic engineering of Yarrowia lipolytica for the production of terpenoids

Ajikumar, 2010, Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli, Science, 330, 70, 10.1126/science.1191652 Alper, 2005, Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets, Nat. Biotechnol., 23, 612, 10.1038/nbt1083 André, 2009, Biotechnological conversions of bio-diesel-derived crude glycerol by Yarrowia lipolytica strains, Eng. Life, 9, 468, 10.1002/elsc.200900063 Attia, 2012, Molecular cloning and characterization of (+)-epi-alpha-bisabolol synthase, catalyzing the first step in the biosynthesis of the natural sweetener, hernandulcin, in Lippia dulcis, Arch. Biochem. Biophys., 527, 37, 10.1016/j.abb.2012.07.010 Bouvier, 2005, Biogenesis, molecular regulation and function of plant isoprenoids, Prog. Lipid Res., 44, 357, 10.1016/j.plipres.2005.09.003 Broker, 2018, Upregulating the mevalonate pathway and repressing sterol synthesis in Saccharomyces cerevisiae enhances the production of triterpenes, Appl. Microbiol. Biotechnol., 102, 6923, 10.1007/s00253-018-9154-7 Burg, 2011, Regulation of HMG-CoA reductase in mammals and yeast, Prog. Lipid Res., 50, 403, 10.1016/j.plipres.2011.07.002 Cao, 2016, Metabolic engineering of oleaginous yeast Yarrowia lipolytica for limonene overproduction, Biotechnol. Biofuels., 9, 214, 10.1186/s13068-016-0626-7 Cao, 2017, Enhancing linalool production by engineering oleaginous yeast Yarrowia lipolytica, Bioresour. Technol., 245, 1641, 10.1016/j.biortech.2017.06.105 Chandran, 2011, Microbial production of isoprenoids, Process Biochem., 46, 1703, 10.1016/j.procbio.2011.05.012 Chang, 2007, Engineering Escherichia coli for production of functionalized terpenoids using plant P450s, Nat. Chem. Biol., 3, 274, 10.1038/nchembio875 Chappell, 1995, Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants, Annu. Rev. Plant Phys., 46, 521, 10.1146/annurev.pp.46.060195.002513 Chen, 2011, The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom, Plant J., 66, 212, 10.1111/j.1365-313X.2011.04520.x Chen, 2015, Enabling technologies to advance microbial isoprenoid production, Adv. Biochem. Eng. Biotechnol., 148, 143 Demissie, 2013, The biosynthetic origin of irregular monoterpenes in Lavandula: isolation and biochemical characterization of a novel cis-prenyl diphosphate synthase gene, lavandulyl diphosphate synthase, J. Biol. Chem., 288, 6333, 10.1074/jbc.M112.431171 Deng, 2016, Enhanced (S)-linalool production by fusion expression of farnesyl diphosphate synthase and linalool synthase in Saccharomyces cerevisiae, J. Appl. Microbiol., 121, 187, 10.1111/jam.13105 Diaz-Chavez, 2013, Biosynthesis of Sandalwood Oil: Santalum album CYP76F cytochromes P450 produce santalols and bergamotol, PLoS One, 8, 10.1371/journal.pone.0075053 Dong, 2018, Co-expression of squalene epoxidases with triterpene cyclases boosts production of triterpenoids in plants and yeast, Metab. Eng., 49, 1, 10.1016/j.ymben.2018.07.002 Gao, 2014, One-step integration of multiple genes into the oleaginous yeast Yarrowia lipolytica, Biotechnol. Lett., 36, 2523, 10.1007/s10529-014-1634-y Gao, 2017, Production of β-carotene by expressing a heterologous multifunctional carotene synthase in Yarrowia lipolytica, Biotechnol. Lett., 39, 921, 10.1007/s10529-017-2318-1 Gao, 2017, Iterative integration of multiple-copy pathway genes in Yarrowia lipolytica for heterologous beta-carotene production, Metab. Eng., 41, 192, 10.1016/j.ymben.2017.04.004 Guerin, 2003, Haematococcus astaxanthin: applications for human health and nutrition, Trends Biotechnol., 21, 210, 10.1016/S0167-7799(03)00078-7 Guo, 2018, Heterologous biosynthesis of (+)-nootkatone in unconventional yeast Yarrowia lipolytica, Biochem. Eng. J., 137, 125, 10.1016/j.bej.2018.05.023 Han, 2018, Ty1-fused protein-body formation for spatial organization of metabolic pathways in Saccharomyces cerevisiae, Biotechnol. Bioeng., 115, 694, 10.1002/bit.26493 Hemmerlin, 2012, A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis?, Prog. Lipid Res., 51, 95, 10.1016/j.plipres.2011.12.001 Ignea, 2014, Engineering monoterpene production in yeast using a synthetic dominant negative geranyl diphosphate synthase, ACS Synth. Biol., 3, 298, 10.1021/sb400115e Jongedijk, 2014, Capturing of the monoterpene olefin limonene produced in Saccharomyces cerevisiae, Yeast, 31, 159 Keeling, 2006, Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens, New Phytol., 170, 657, 10.1111/j.1469-8137.2006.01716.x Khersonsky, 2006, Enzyme promiscuity: evolutionary and mechanistic aspects, Curr. Opin. Chem. Biol., 10, 498, 10.1016/j.cbpa.2006.08.011 Kildegaard, 2017, Engineering of Yarrowia lipolytica for production of astaxanthin, Synth. Syst. Biotechnol., 2, 287, 10.1016/j.synbio.2017.10.002 King, J., Edgar, S., Qiao, K., Stephanopoulos, G. 2016. Accessing Nature's diversity through metabolic engineering and synthetic biology. F1000Res. 5. Kong, 2019, Efficient l-lactic acid production from corncob residue using metabolically engineered thermo-tolerant yeast, Bioresour. Technol., 273, 220, 10.1016/j.biortech.2018.11.018 Kuranda, 2010, The isoprenoid pathway and transcriptional response to its inhibitors in the yeast Saccharomyces cerevisiae, FEMS Yeast Res., 10, 14, 10.1111/j.1567-1364.2009.00560.x Lange, 2013, Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities, Plant Biotechnol. J., 11, 169, 10.1111/pbi.12022 Larroude, 2018, A synthetic biology approach to transform Yarrowia lipolytica into a competitive biotechnological producer of β-carotene, Biotechnol. Bioeng., 115, 464, 10.1002/bit.26473 Li, 2019, Production of triterpene ginsenoside compound K in the nonconventional yeast Yarrowia lipolytica, J. Agric. Food. Chem. Li, 2016, Enabling xylose utilization in Yarrowia lipolytica for lipid production, Biotechnol. J., 11, 1230, 10.1002/biot.201600210 Li, 2019, Improving lycopene production in Saccharomyces cerevisiae through optimizing pathway and chassis metabolism, Chem. Eng. Sci., 193, 364, 10.1016/j.ces.2018.09.030 Liu, 2018, Engineering and manipulation of a mevalonate pathway in Escherichia coli for isoprene production, Appl. Microbiol. Biotechnol., 103, 239, 10.1007/s00253-018-9472-9 Liu, 2017, Engineering Yarrowia lipolytica for arachidonic acid production through rapid assembly of metabolic pathway, Biochem. Eng. J., 119, 52, 10.1016/j.bej.2016.12.004 Liu, 2017, A Yarrowia lipolytica strain engineered for arachidonic acid production counteracts metabolic burden by redirecting carbon flux towards intracellular fatty acid accumulation at the expense of or ganic acids secretion, Biochem. Eng. J., 128, 201, 10.1016/j.bej.2017.10.007 Liu, 2015, Biotechnological applications of Yarrowia lipolytica: Past, present and future, Biotechnol. Adv., 33, 1522, 10.1016/j.biotechadv.2015.07.010 Liu, 2017, Protein and metabolic engineering for the production of organic acids, Bioresour. Technol., 239, 412, 10.1016/j.biortech.2017.04.052 Lombard, 2011, Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life, Mol. Biol. Evol., 28, 87, 10.1093/molbev/msq177 Maimone, 2007, Modern synthetic efforts toward biologically active terpenes, Nat. Chem. Biol., 3, 396, 10.1038/nchembio.2007.1 Mata-Gómez, 2014, Biotechnological production of carotenoids by yeasts: an overview, Microb. Cell Fact., 13, 12, 10.1186/1475-2859-13-12 Matthaus, 2014, Production of lycopene in the non-carotenoid-producing yeast Yarrowia lipolytica, Appl. Environ. Microbiol., 80, 1660, 10.1128/AEM.03167-13 Milani, 2017, Carotenoids: biochemistry, pharmacology and treatment, Br. J. Pharmacol., 174, 1290, 10.1111/bph.13625 Nambou, 2015, Flux balance analysis inspired bioprocess upgrading for lycopene production by a metabolically engineered strain of Yarrowia lipolytica, Metabolites, 5, 794, 10.3390/metabo5040794 Pateraki, 2015, Cytochromes P450 for Terpene Functionalisation and Metabolic Engineering, 107 Peng, 2018, Engineered protein degradation of farnesyl pyrophosphate synthase is an effective regulatory mechanism to increase monoterpene production in Saccharomyces cerevisiae, Metab. Eng., 47, 83, 10.1016/j.ymben.2018.02.005 Peng, 2017, A squalene synthase protein degradation method for improved sesquiterpene production in Saccharomyces cerevisiae, Metab. Eng., 39, 209, 10.1016/j.ymben.2016.12.003 Polakowski, 1998, Overexpression of a cytosolic hydroxymethylglutaryl-CoA reductase leads to squalene accumulation in yeast, Appl. Microbiol. Biotechnol., 49, 66, 10.1007/s002530051138 Ribeiro, 2018, Antioxidant and pro-oxidant activities of carotenoids and their oxidation products, Food Chem. Toxicol., 120, 681, 10.1016/j.fct.2018.07.060 Ro, 2006, Production of the antimalarial drug precursor artemisinic acid in engineered yeast, Nature, 440, 940, 10.1038/nature04640 Roberts, 2007, Production and engineering of terpenoids in plant cell culture, Nat. Chem. Biol., 3, 387, 10.1038/nchembio.2007.8 Rodriguez, 2017, Metabolic engineering of yeast for fermentative production of flavonoids, Bioresour. Technol., 245, 1645, 10.1016/j.biortech.2017.06.043 Schempp, 2017, Microbial cell factories for the production of terpenoid flavor and fragrance compounds, J. Agr. Food Chem., 66, 2247, 10.1021/acs.jafc.7b00473 Schwartz, 2017, Host and pathway engineering for enhanced lycopene biosynthesis in Yarrowia lipolytica, Front. Microbiol., 8, 2233, 10.3389/fmicb.2017.02233 Shi, 2018, Advancing metabolic engineering of Yarrowia lipolytica using the CRISPR/Cas system, Appl. Microbiol. Biotechnol., 102, 9541, 10.1007/s00253-018-9366-x Sun, 2018, Glycerol improves heterologous biosynthesis of betulinic acid in engineered Yarrowia lipolytica, Chem. Eng. Sci., 196, 82, 10.1016/j.ces.2018.10.052 Sun, 2017, Engineering Yarrowia lipolytica for efficient γ-linolenic acid production, Biochem. Eng. J., 117, 172, 10.1016/j.bej.2016.10.014 Tanaka, 2018, Mannosylinositol phosphorylceramides and ergosterol coodinately maintain cell wall integrity in the yeast Saccharomyces cerevisiae, FEBS J., 285, 2405, 10.1111/febs.14509 Tholl, 2006, Terpene synthases and the regulation, diversity and biological roles of terpene metabolism, Curr. Opin. Plant Biol., 9, 297, 10.1016/j.pbi.2006.03.014 Tippmann, 2017, Affibody scaffolds improve sesquiterpene production in Saccharomyces cerevisiae, ACS Synth. Biol., 6, 19, 10.1021/acssynbio.6b00109 Ukibe, 2009, Metabolic engineering of Saccharomyces cerevisiae for astaxanthin production and oxidative stress tolerance, Appl. Environ. Microbiol., 75, 7205, 10.1128/AEM.01249-09 Wang, 2018, Microbial platform for terpenoid production: Escherichia coli and yeast, Front. Microbiol., 9, 2460, 10.3389/fmicb.2018.02460 Wang, 2017, Metabolic engineering and synthetic biology approaches driving isoprenoid production in Escherichia coli, Bioresour. Technol., 241, 430, 10.1016/j.biortech.2017.05.168 Wu, 2018, Engineering Saccharomyces cerevisiae for the production of the valuable monoterpene ester geranyl acetate, Microb. Cell Fact., 17, 85, 10.1186/s12934-018-0930-y Yan, 2012, Enhancement of beta-carotene production by over-expression of HMG-CoA reductase coupled with addition of ergosterol biosynthesis inhibitors in recombinant Saccharomyces cerevisiae, Curr. Microbiol., 64, 159, 10.1007/s00284-011-0044-9 Yan, 2014, Production of bioactive ginsenoside compound K in metabolically engineered yeast, Cell Res., 24, 770, 10.1038/cr.2014.28 Yang, 2016, Heterologous production of α-farnesene in metabolically engineered strains of Yarrowia lipolytica, Bioresour. Technol., 216, 1040, 10.1016/j.biortech.2016.06.028 Zeng, 2018, Recent advances in metabolic engineering of Yarrowia lipolytica for lipid overproduction, Eur. J. Lipid Sci. Tech., 120, 1700352, 10.1002/ejlt.201700352 Zhang, 2017, Engineering yeast metabolism for production of terpenoids for use as perfume ingredients, pharmaceuticals and biofuels, FEMS Yeast Res., 17, 1, 10.1093/femsyr/fox080 Zhao, 2017, Metabolomic changes and metabolic responses to expression of heterologous biosynthetic genes for lycopene production in Yarrowia lipolytica, J. Biotechnol., 251, 174, 10.1016/j.jbiotec.2017.04.019 Zhou, 2018, Expanding the terpenoid kingdom, Nat. Chem. Biol., 14, 1069, 10.1038/s41589-018-0167-4 Zhu, 2015, Metabolic engineering of Yarrowia lipolytica for industrial applications, Curr. Opin. Biotechnol., 36, 65, 10.1016/j.copbio.2015.08.010