Strategies at Bioreactor Scale for the Production of Recombinant Proteins in Yarrowia lipolytica

Vandermies, Marie; Fickers, Patrick

doi:10.1007/978-3-030-21110-3_16

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Strategies at Bioreactor Scale for the Production of Recombinant Proteins in Yarrowia lipolytica

Vandermies, Marie; Fickers, Patrick

2019 • In Sibirny, Andriy (Ed.) Non-conventional Yeasts: from Basic Research to Application

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https://hdl.handle.net/2268/239061

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10.1007/978-3-030-21110-3_16

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Keywords :

Yarrowia lipolytica; Recombinant protein; Bioreactor; Metabolic load; Molecular strategies; Process strategies

Abstract :

[en] Recombinant protein production represents a multibillion-dollar market. Therefore, it constitutes an important research field both in academia and industry. The use of yeast as cell factory presents several advantages such as ease of genetic manipulation, growth at high cell density, and possibility of posttranslational modifications. Yarrowia lipolytica is considered as one of the most attractive hosts due to its ability to metabolize raw substrate, to express genes at high level, and to secrete protein in large amounts. In the recent years, several reviews were dedicated to genetic tools developed for this purpose. Although the construction of efficient cell factory for recombinant protein synthesis is important, the development of an efficient process for protein production constitutes an equally vital aspect. Indeed, a sports car could not drive fast on a gravel road. The aim of this review is to provide a comprehensive snapshot of process tools to consider for recombinant protein production in bioreactor using Y. lipolytica as a cell factory, in order to facilitate the decision-making for future strain and process engineering.

Disciplines :

Biotechnology

Author, co-author :

Vandermies, Marie ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbial, food and biobased technologies

Fickers, Patrick ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbial, food and biobased technologies

Language :

English

Title :

Strategies at Bioreactor Scale for the Production of Recombinant Proteins in Yarrowia lipolytica

Publication date :

12 September 2019

Main work title :

Non-conventional Yeasts: from Basic Research to Application

Author, co-author :

Sibirny, Andriy

Publisher :

Springer

Funders :

FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture

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since 01 September 2019

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Bibliography

Aloulou A, Rodriguez JA, Puccinelli D et al (2007) Purification and biochemical characterization of the LIP2 lipase from Yarrowia lipolytica. Biochim Biophys Acta BBA - Mol Cell Biol Lipids 1771:228-237. https://doi.org/10.1016/j.bbalip.2006.12.006
Amaral PFF, Freire MG, Rocha-Leão MHM et al (2008) Optimization of oxygen mass transfer in a multiphase bioreactor with perfluorodecalin as a second liquid phase. Biotechnol Bioeng 99:588-598. https://doi.org/10.1002/bit.21640
Angov E (2011) Codon usage: Nature’s roadmap to expression and folding of proteins. Biotechnol J 6:650-659. https://doi.org/10.1002/biot.201000332
Babour A, Kabani M, Boisramé A, Beckerich J-M (2008) Characterization of Ire1 in the yeast Yarrowia lipolytica reveals an important role for the Sls1 nucleotide exchange factor in unfolded protein response regulation. Curr Genet 53:337. https://doi.org/10.1007/s00294-008-0190-1
Barth G, Gaillardin C (1996) Yarrowia lipolytica. In: Nonconventional Yeasts in Biotechnology. Springer, Berlin/Heidelberg, pp 313-388
Bellou S, Makri A, Triantaphyllidou I-E et al (2014) Morphological and metabolic shifts of Yarrowia lipolytica induced by alteration of the dissolved oxygen concentration in the growth environment. Microbiology 160:807-817. https://doi.org/10.1099/mic.0.074302-0
Bhave SL, Chattoo BB (2003) Expression of Vitreoscilla hemoglobin improves growth and levels of extracellular enzyme in Yarrowia lipolytica. Biotechnol Bioeng 84:658-666. https://doi. org/10.1002/bit.10817
Biryukova EN, Medentsev AG, Arinbasarova AY, Akimenko VK (2006) Tolerance of the yeast Yarrowia lipolytica to oxidative stress. Microbiology 75:243-247. https://doi.org/10.1134/S0026261706030015
Blazeck J, Liu L, Redden H, Alper H (2011) Tuning gene expression in Yarrowia lipolytica by a hybrid promoter approach. Appl Environ Microbiol 77:7905-7914. https://doi.org/10.1128/AEM.05763-11
Blazeck J, Reed B, Garg R et al (2013) Generalizing a hybrid synthetic promoter approach in Yarrowia lipolytica. Appl Microbiol Biotechnol 97:3037-3052. https://doi.org/10.1007/s00253-012-4421-5
Bordes F, Fudalej F, Dossat V et al (2007) A new recombinant protein expression system for high-throughput screening in the yeast Yarrowia lipolytica. J Microbiol Methods 70:493-502. https://doi.org/10.1016/j.mimet.2007.06.008
Borsenberger V, Onésime D, Lestrade D et al (2018) Multiple parameters drive the efficiency of CRISPR/Cas9-induced gene modifications in Yarrowia lipolytica. J Mol Biol 430:4293-4306. https://doi.org/10.1016/j.jmb.2018.08.024
Botes AL, Labuschagne M, Roth R, et al (2008) Recombinant Yeasts for Synthesizing Epoxide Hydrolases. U.S. patent, US 20080171359 A1
Bouchedja DN, Danthine S, Kar T et al (2017) Online flow cytometry, an interesting investigation process for monitoring lipid accumulation, dimorphism, and cells’ growth in the oleaginous yeast Yarrowia lipolytica JMY 775. Bioresour Bioprocess 4:3. https://doi.org/10.1186/s40643-016-0132-6
Callewaert NLM, Vervecken W, Pourcq KJMD, et al (2009) Yarrowia lipolytica and Pichia pastoris HAC1 nucleic acids U.S. Patent, US20090069232A1.
Carly F, Steels S, Telek S et al (2018) Identification and characterization of EYD1, encoding an erythritol dehydrogenase in Yarrowia lipolytica and its application to bioconvert erythritol into erythrulose. Bioresour Technol 247:963-969. https://doi.org/10.1016/j.biortech.2017.09.168
Celińska E, Nicaud J-M (2018) Filamentous fungi-like secretory pathway strayed in a yeast system:peculiarities of Yarrowia lipolytica secretory pathway underlying its extraordinary performance. Appl Microbiol Biotechnol 103(1):39-52. https://doi.org/10.1007/s00253-018-9450-2
Celińska E, Białas W, Borkowska M, Grajek W (2015) Cloning, expression, and purification of insect (Sitophilus oryzae) alpha-amylase, able to digest granular starch, in Yarrowia lipolytica host. Appl Microbiol Biotechnol 99:2727-2739. https://doi.org/10.1007/s00253-014-6314-2
Celińska E, Borkowska M, Białas W (2016) Evaluation of heterologous α-amylase production in two expression platforms dedicated for Yarrowia lipolytica: commercial Po1g-pYLSC (php4d) and custom-made A18-pYLTEF (pTEF). Yeast 33:165-181. https://doi.org/10.1002/yea.3149
Celińska E, Borkowska M, Białas W (2017) Enhanced production of insect raw-starch-digesting alpha-amylase accompanied by high erythritol synthesis in recombinant Yarrowia lipolytica fed-batch cultures at high-cell-densities. Process Biochem 52:78-85. https://doi.org/10.1016/j. procbio.2016.10.022
Celińska E, Borkowska M, Białas W et al (2018) Robust signal peptides for protein secretion in Yarrowia lipolytica: identification and characterization of novel secretory tags. Appl Microbiol Biotechnol 102:5221-5233. https://doi.org/10.1007/s00253-018-8966-9
Cervantes-Chávez JA, Ruiz-Herrera J (2006) STE11 disruption reveals the central role of a MAPK pathway in dimorphism and mating in Yarrowia lipolytica. FEMS Yeast Res 6:801-815. https:// doi.org/10.1111/j.1567-1364.2006.00084.x
Cervantes-Chávez JA, Kronberg F, Passeron S, Ruiz-Herrera J (2009) Regulatory role of the PKA pathway in dimorphism and mating in Yarrowia lipolytica. Fungal Genet Biol 46:390-399. https://doi.org/10.1016/j.fgb.2009.02.005
Chang CC, Ryu DDY, Park CS, Kim J-Y (1997) Enhancement of rice α-amylase production in recombinant Yarrowia lipolytica. J Ferment Bioeng 84:421-427. https://doi.org/10.1016/S0922-338X(97)82002-8
Chang CC, Ryu DDY, Park CS, Kim J-Y (1998a) Improvement of heterologous protein productivity using recombinant Yarrowia lipolytica and cyclic fed-batch process strategy. Biotechnol Bioeng 59:379-385. https://doi.org/10.1002/ (SICI)1097-0290(19980805)59:3<379::AID-BIT15>3.0.CO;2-9
Chang CC, Ryu DDY, Park CS et al (1998b) Recombinant bioprocess optimization for heterologous protein production using two-stage, cyclic fed-batch culture. Appl Microbiol Biotechnol 49:531-537. https://doi.org/10.1007/s002530051209
Chang J, Fagarasanu A, Rachubinski RA (2007) Peroxisomal Peripheral Membrane Protein YlInp1p Is Required for Peroxisome Inheritance and Influences the Dimorphic Transition in the Yeast Yarrowia lipolytica. Eukaryot Cell 6:1528-1537. https://doi.org/10.1128/EC.00185-07
Coelho MAZ, Amaral PFF, Belo I (2010) Yarrowia lipolytica: an industrial workhorse. In: Méndez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology advances. Formatex Research Center, pp 930-940
Corchero JL, Villaverde A (1998) Plasmid maintenance in Escherichia coli recombinant cultures is dramatically, steadily, and specifically influenced by features of the encoded proteins. Biotechnol Bioeng 58:625-632. https://doi.org/10.1002/ (SICI)1097-0290(19980620)58:6625::AID-BIT83.0.CO;2-K
Cui W, Wang Q, Zhang F et al (2011) Direct conversion of inulin into single cell protein by the engineered Yarrowia lipolytica carrying inulinase gene. Process Biochem 46:1442-1448. https://doi.org/10.1016/j.procbio.2011.03.017
Darvishi F, Moradi M, Madzak C, Jolivalt C (2017) Production of Laccase by Recombinant Yarrowia lipolytica from Molasses: Bioprocess Development Using Statistical Modeling and Increase Productivity in Shake-Flask and Bioreactor Cultures. Appl Biochem Biotechnol 181:1228-1239. https://doi.org/10.1007/s12010-016-2280-8
Darvishi F, Moradi M, Jolivalt C, Madzak C (2018) Laccase production from sucrose by recombinant Yarrowia lipolytica and its application to decolorization of environmental pollutant dyes. Ecotoxicol Environ Saf 165:278-283. https://doi.org/10.1016/j.ecoenv.2018.09.026
De Pourcq K, Vervecken W, Dewerte I et al (2012a) Engineering the yeast Yarrowia lipolytica for the production of therapeutic proteins homogeneously glycosylated with Man8GlcNAc2 and Man5GlcNAc2. Microb Cell Factories 11:53. https://doi.org/10.1186/1475-2859-11-53
De Pourcq K, Tiels P, Hecke AV et al (2012b) Engineering Yarrowia lipolytica to Produce Glycoproteins Homogeneously Modified with the Universal Man3GlcNAc2 N-Glycan Core. PLOS ONE 7:e39976. https://doi.org/10.1371/journal.pone.0039976
de Ruijter JC, Koskela EV, Nandania J et al (2018) Understanding the metabolic burden of recombinant antibody production in Saccharomyces cerevisiae using a quantitative metabolomics approach. Yeast 35:331-341. https://doi.org/10.1002/yea.3298
Delvigne F, Zune Q, Lara AR et al (2014) Metabolic variability in bioprocessing: implications of microbial phenotypic heterogeneity. Trends Biotechnol 32:608-616. https://doi.org/10.1016/j. tibtech.2014.10.002
Dulermo R, Brunel F, Dulermo T et al (2017) Using a vector pool containing variable-strength promoters to optimize protein production in Yarrowia lipolytica. Microb Cell Factories 16(1):31. https://doi.org/10.1186/s12934-017-0647-3
Egermeier M, Russmayer H, Sauer M, Marx H (2017) Metabolic flexibility of Yarrowia lipolytica growing on glycerol. Front Microbiol 8:49. https://doi.org/10.3389/fmicb.2017.00049
Emond S, Montanier C, Nicaud J-M et al (2010) New efficient recombinant expression system to engineer Candida antarctica lipase B. Appl Environ Microbiol 76:2684-2687. https://doi. org/10.1128/AEM.03057-09
Fickers P, Le Dall M, Gaillardin C et al (2003) New disruption cassettes for rapid gene disruption and marker rescue in the yeast Yarrowia lipolytica. J Microbiol Methods 55:727-737. https:// doi.org/10.1016/j.mimet.2003.07.003
Fickers P, Nicaud JM, Gaillardin C et al (2004) Carbon and nitrogen sources modulate lipase production in the yeast Yarrowia lipolytica. J Appl Microbiol 96:742-749. https://doi. org/10.1111/j.1365-2672.2004.02190.x
Fickers P, Destain J, Thonart P (2005a) Methyl oleate modulates LIP2 expression in the lipolytic yeast Yarrowia lipolytica. Biotechnol Lett 27:1751-1754. https://doi.org/10.1007/s10529-005-3547-2
Fickers P, Fudalej F, Dall MTL et al (2005b) Identification and characterisation of LIP7 and LIP8 genes encoding two extracellular triacylglycerol lipases in the yeast Yarrowia lipolytica. Fungal Genet Biol 42:264-274. https://doi.org/10.1016/j.fgb.2004.12.003
Fickers P, Fudalej F, Nicaud J-M et al (2005c) Selection of new over-producing derivatives for the improvement of extracellular lipase production by the non-conventional yeast Yarrowia lipolytica. J Biotechnol 115:379-386. https://doi.org/10.1016/j.jbiotec.2004.09.014
Fickers P, Destain J, Thonart P (2009) Improvement of Yarrowia lipolytica lipase production by fed-batch fermentation. J Basic Microbiol 49:212-215. https://doi.org/10.1002/jobm.200800186
Fickers P, Marty A, Nicaud JM (2011) The lipases from Yarrowia lipolytica: genetics, production, regulation, biochemical characterization and biotechnological applications. Biotechnol Adv 29:632-644. https://doi.org/10.1016/j.biotechadv.2011.04.005
Förster A, Aurich A, Mauersberger S, Barth G (2007) Citric acid production from sucrose using a recombinant strain of the yeast Yarrowia lipolytica. Appl Microbiol Biotechnol 75:1409-1417. https://doi.org/10.1007/s00253-007-0958-0
Gao S, Tong Y, Wen Z et al (2016) Multiplex gene editing of the Yarrowia lipolytica genome using the CRISPR-Cas9 system. J Ind Microbiol Biotechnol 43:1085-1093. https://doi.org/10.1007/s10295-016-1789-8
Gasmi N, Ayed A, Nicaud J-M, Kallel H (2011a) Design of an efficient medium for heterologous protein production in Yarrowia lipolytica: case of human interferon alpha 2b. Microb Cell Factories 10:38
Gasmi N, Ayed A, Ammar BBH et al (2011b) Development of a cultivation process for the enhancement of human interferon alpha 2b production in the oleaginous yeast, Yarrowia lipolytica. Microb Cell Factories 10:90. https://doi.org/10.1186/1475-2859-10-90
Gasmi N, Lassoued R, Ayed A et al (2012) Production and characterization of human granulocyte- macrophage colony-stimulating factor (hGM-CSF) expressed in the oleaginous yeast Yarrowia lipolytica. Appl Microbiol Biotechnol 96:89-101. https://doi.org/10.1007/s00253-012-4141-x
Glick BR (1995) Metabolic load and heterologous gene expression. Biotechnol Adv 13:247-261. https://doi.org/10.1016/0734-9750(95)00004-A
Görgens JF, van Zyl WH, Knoetze JH, Hahn-Hägerdal B (2001) The metabolic burden of the PGK1 and ADH2 promoter systems for heterologous xylanase production by Saccharomyces cerevisiae in defined medium. Biotechnol Bioeng 73:238-245. https://doi.org/10.1002/bit.1056
Groenewald M, Boekhout T, Neuvéglise C et al (2014) Yarrowia lipolytica: safety assessment of an oleaginous yeast with a great industrial potential. Crit Rev Microbiol 40:187-206. https:// doi.org/10.3109/1040841X.2013.770386
Guo Z, Robin J, Duquesne S et al (2018) Developing cellulolytic Yarrowia lipolytica as a platform for the production of valuable products in consolidated bioprocessing of cellulose. Biotechnol Biofuels 11:141. https://doi.org/10.1186/s13068-018-1144-6
Hamsa PV, Chattoo BB (1994) Cloning and growth-regulated expression of the gene encoding the hepatitis B virus middle surface antigen in Yarrowia lipolytica. Gene 143:165-170. https://doi. org/10.1016/0378-1119(94)90092-2
Hanquier J, Sorlet Y, Desplancq D et al (2003) A single mutation in the activation site of bovine trypsinogen enhances its accumulation in the fermentation broth of the yeast Pichia pastoris. Appl Environ Microbiol 69:1108-1113. https://doi.org/10.1128/AEM.69.2.1108-1113.2003
Heslot H, Nicaud JM, Fabre E et al (1990) Cloning of the alkaline extracellular protease gene of Yarrowia lipolytica and its use to express foreign genes. In: Nga BH, Lee YK (eds) Microbiological application in food biotechnology. Elsevier, Amsterdam, pp 27-45
Holkenbrink C, Dam MI, Kildegaard KR et al (2018) EasyCloneYALI: CRISPR/Cas9-based synthetic toolbox for engineering of the yeast Yarrowia lipolytica. Biotechnol J 13:1700543. https://doi.org/10.1002/biot.201700543
Huang Y-C, Chen Y-F, Chen C-Y et al (2011) Production of ferulic acid from lignocellulolytic agricultural biomass by Thermobifida fusca thermostable esterase produced in Yarrowia lipolytica transformant. Bioresour Technol 102:8117-8122. https://doi.org/10.1016/j. biortech.2011.05.062
Huang Y-Y, Jian X-X, Lv Y-B et al (2018) Enhanced squalene biosynthesis in Yarrowia lipolytica based on metabolically engineered acetyl-CoA metabolism. J Biotechnol 281:106-114. https:// doi.org/10.1016/j.jbiotec.2018.07.001
Hurtado CA, Rachubinski RA (1999) MHY1 encodes a C2H2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica. J Bacteriol 181:3051-3057
Hurtado CAR, Rachubinski RA (2002a) Isolation and Characterization of YlBEM1, a Gene Required for Cell Polarization and Differentiation in the Dimorphic Yeast Yarrowia lipolytica. Eukaryot Cell 1:526-537. https://doi.org/10.1128/EC.1.4.526-537.2002
Hurtado CAR, Rachubinski RA (2002b) YlBMH1 encodes a 14-3-3 protein that promotes filamentous growth in the dimorphic yeast Yarrowia lipolytica. Microbiology 148:3725-3735. https:// doi.org/10.1099/00221287-148-11-3725
Hurtado CAR, Beckerich J-M, Gaillardin C, Rachubinski RA (2000) A Rac Homolog Is Required for Induction of Hyphal Growth in the Dimorphic Yeast Yarrowia lipolytica. J Bacteriol 182:2376-2386. https://doi.org/10.1128/JB.182.9.2376-2386.2000
Jaafar L, León M, Zueco J (2003) Isolation of the MNN9 gene of Yarrowia lipolytica (YlMNN9) and phenotype analysis of a mutant ylmnn9δ strain. Yeast 20:633-644. https://doi.org/10.1002/yea.990
James LC, Strick CA (1998) Multiple integrative vectors and Yarrowia lipolytica transformants. U.S. patent, US5786212A
Jolivet P, Bordes F, Fudalej F et al (2007) Analysis of Yarrowia lipolytica extracellular lipase Lip2p glycosylation. FEMS Yeast Res 7:1317-1327. https://doi. org/10.1111/j.1567-1364.2007.00293.x
Juretzek T, Wang H-J, Nicaud J-M et al (2000) Comparison of promoters suitable for regulated overexpression of β-galactosidase in the alkane-utilizing yeastYarrowia lipolytica. Biotechnol Bioprocess Eng 5:320-326. https://doi.org/10.1007/BF02942206
Juretzek T, Le Dall M-T, Mauersberger S et al (2001) Vectors for gene expression and amplification in the yeast Yarrowia lipolytica. Yeast 18:97-113. https://doi. org/10.1002/1097-0061(20010130)18:297::AID-YEA6523.0.CO;2-U
Kar T, Delvigne F, Masson M et al (2008) Investigation of the effect of different extracellular factors on the lipase production by Yarrowia lipolytica on the basis of a scale-down approach. J Ind Microbiol Biotechnol 35:1053-1059. https://doi.org/10.1007/s10295-008-0382-1
Kar T, Delvigne F, Destain J, Thonart P (2011) Bioreactor scale-up and design on the basis of physiologically relevant parameters: application to the production of lipase by Yarrowia lipolytica. Biotechnol Agron Soc Env 11
Kar T, Destain J, Thonart P, Delvigne F (2012) Scale-down assessment of the sensitivity of Yarrowia lipolytica to oxygen transfer and foam management in bioreactors: investigation of the underlying physiological mechanisms. J Ind Microbiol Biotechnol 39:337-346. https://doi. org/10.1007/s10295-011-1030-8
Katre G, Ajmera N, Zinjarde S, RaviKumar A (2017) Mutants of Yarrowia lipolytica NCIM 3589 grown on waste cooking oil as a biofactory for biodiesel production. Microb Cell Factories 16. https://doi.org/10.1186/s12934-017-0790-x
Kebabci Ö, Cihangir N (2012) Comparison of three Yarrowia lipolytica strains for lipase production:NBRC 1658, IFO 1195, and a local strain. Turk J Biol 36:15-24
Kim J-W, Park TJ, Ryu DDY, Kim J-Y (2000) High cell density culture of Yarrowia lipolytica using a one-step feeding process. Biotechnol Prog 16:657-660. https://doi.org/10.1021/bp000037n
Kopečný D, Pethe C, Šebela M et al (2005) High-level expression and characterization of Zea mays cytokinin oxidase/dehydrogenase in Yarrowia lipolytica. Biochimie 87:1011-1022. https://doi. org/10.1016/j.biochi.2005.04.006
Kraiem H, Manon Y, Anne-Archard D, Fillaudeau L (2013) In-situ and ex-situ rheometry of high density Yarrowia lipolytica broth: determination of critical concentration and impact of yeast mycelial transition. In Proceedings of the 48ème congrès annuel du Groupe Français de Rhéologie-GFR 2013, Nantes, France, 28 October-30 October 2013.
Lazar Z, Gamboa-Meléndez H, Le Coq A-MC-, et al (2015) Awakening the endogenous Leloir pathway for efficient galactose utilization by Yarrowia lipolytica. Biotechnol Biofuels 8:185. https://doi.org/10.1186/s13068-015-0370-4
Lazar Z, Rossignol T, Verbeke J et al (2013) Optimized invertase expression and secretion cassette for improving Yarrowia lipolytica growth on sucrose for industrial applications. J Ind Microbiol Biotechnol 40:1273-1283. https://doi.org/10.1007/s10295-013-1323-1
Le Dall M-T, Nicaud J-M, Gaillardin C (1994) Multiple-copy integration in the yeast Yarrowia lipolytica. Curr Genet 26:38-44. https://doi.org/10.1007/BF00326302
Ledesma-Amaro R, Dulermo T, Nicaud JM (2015) Engineering Yarrowia lipolytica to produce biodiesel from raw starch. Biotechnol Biofuels 8:1
Ledesma-Amaro R, Lazar Z, Rakicka M et al (2016) Metabolic engineering of Yarrowia lipolytica to produce chemicals and fuels from xylose. Metab Eng 38:115-124. https://doi.org/10.1016/j. ymben.2016.07.001
Li H, Alper HS (2016) Enabling xylose utilization in Yarrowia lipolytica for lipid production. Biotechnol J 11:1230-1240. https://doi.org/10.1002/biot.201600210
Li M, Li Y-Q, Zhao X-F, Gao X-D (2014) Roles of the three Ras proteins in the regulation of dimorphic transition in the yeast Yarrowia lipolytica. FEMS Yeast Res 14:451-463. https://doi. org/10.1111/1567-1364.12129
Li C, Gao S, Yang X, Lin CSK (2018a) Green and sustainable succinic acid production from crude glycerol by engineered Yarrowia lipolytica via agricultural residue based in situ fibrous bed bioreactor. Bioresour Technol 249:612-619. https://doi.org/10.1016/j.biortech.2017.10.011
Li C, Gao S, Li X et al (2018b) Efficient metabolic evolution of engineered Yarrowia lipolytica for succinic acid production using a glucose-based medium in an in situ fibrous bioreactor under low-pH condition. Biotechnol Biofuels 11:236. https://doi.org/10.1186/s13068-018-1233-6
Liu S, Wan D, Wang M et al (2015) Overproduction of pro-transglutaminase from Streptomyces hygroscopicus in Yarrowia lipolytica and its biochemical characterization. BMC Biotechnol 15. https://doi.org/10.1186/s12896-015-0193-1
Loira N, Dulermo T, Nicaud J-M, Sherman DJ (2012) A genome-scale metabolic model of the lipid-accumulating yeast Yarrowia lipolytica. BMC Syst Biol 6:35. https://doi. org/10.1186/1752-0509-6-35
Lopes M, Gomes N, Mota M, Belo I (2009) Yarrowia lipolytica growth under increased air pressure:influence on enzyme production. Appl Biochem Biotechnol 159:46-53. https://doi. org/10.1007/s12010-008-8359-0
Lopes M, Mota M, Belo I (2013) Comparison of Yarrowia lipolytica and Pichia pastoris Cellular Response to Different Agents of Oxidative Stress. Appl Biochem Biotechnol 170:448-458. https://doi.org/10.1007/s12010-013-0205-3
Madzak C (2003) New tools for heterologous protein production in the yeast Yarrowia lipolytica. In: Pandalai SG (ed) Recent research developments in microbiology. Research Signpost, Trivandrum, pp 453-479
Madzak C, Beckerich J-M (2013) Heterologous protein expression and secretion in Yarrowia lipolytica. In: Barth G (ed) Yarrowia lipolytica. Springer, Berlin Heidelberg, pp 1-76
Madzak C, Tréton B, Blanchin-Roland S (2000) Strong hybrid promoters and integrative expression/secretion vectors for quasi-constitutive expression of heterologous proteins in the yeast Yarrowia lipolytica. J Mol Microbiol Biotechnol 2:207-216
Madzak C, Otterbein L, Chamkha M et al (2005) Heterologous production of a laccase from the basidiomycete Pycnoporus cinnabarinus in the dimorphic yeast Yarrowia lipolytica. FEMS Yeast Res 5:635-646. https://doi.org/10.1016/j.femsyr.2004.10.009
Maharajh D, Roth R, Lalloo R et al (2008a) Multi-copy expression and fed-batch production of Rhodotorula araucariae epoxide hydrolase in Yarrowia lipolytica. Appl Microbiol Biotechnol 79:235-244. https://doi.org/10.1007/s00253-008-1420-7
Maharajh D, Lalloo R, Görgens J (2008b) Effect of an exponential feeding regime on the production of Rhodotorula araucariae epoxide hydrolase in Yarrowia lipolytica. Lett Appl Microbiol 47:520-525. https://doi.org/10.1111/j.1472-765X.2008.02425.x
Mattanovich D, Branduardi P, Dato L et al (2012) Recombinant protein production in yeasts. In:Lorence A (ed) Recombinant gene expression. Humana Press, Totowa, pp 329-358
Mishra P, Lee N-R, Lakshmanan M et al (2018) Genome-scale model-driven strain design for dicarboxylic acid production in Yarrowia lipolytica. BMC Syst Biol 12(Suppl 2):12. https:// doi.org/10.1186/s12918-018-0542-5
Morales-Vargas AT, Domínguez A, Ruiz-Herrera J (2012) Identification of dimorphism-involved genes of Yarrowia lipolytica by means of microarray analysis. Res Microbiol 163:378-387. https://doi.org/10.1016/j.resmic.2012.03.002
Müller S, Dalbøge H (2001) Yeast promoters suitable for expression cloning in yeast and heterologous expression of proteins in yeast. U.S. patent, US6265185.
Nicaud J-M (2012) Yarrowia lipolytica. Yeast 29:409-418. https://doi.org/10.1002/yea.2921
Nicaud J-M, Fabre E, Gaillardin C (1989) Expression of invertase activity in Yarrowia lipolytica and its use as a selective marker. Curr Genet 16:253-260. https://doi.org/10.1007/BF00422111
Nicaud J, Madzak C, Vandenbroek P et al (2002) Protein expression and secretion in the yeast Yarrowia lipolytica. FEMS Yeast Res 2:371-379. https://doi.org/10.1016/S1567-1356(02)00082-X
Nicaud J-M, Trassaert M, Thomas S, et al (2018) Inducible promoter for gene expression and synthetic biology. World patent application, WO2018210867 A1
Ogrydziak DM, Scharf SJ (1982) Alkaline extracellular protease produced by Saccharomycopsis lipolytica CX161-1B. J Gen Microbiol 128:1225-1234. https://doi. org/10.1099/00221287-128-6-1225
Oh MH, Cheon SA, Kang HA, Kim J-Y (2010) Functional characterization of the unconventional splicing of Yarrowia lipolytica HAC1 mRNA induced by unfolded protein response. Yeast 27:443-452. https://doi.org/10.1002/yea.1762
Palande AS, Kulkarni SV, León-Ramirez C et al (2014) Dimorphism and hydrocarbon metabolism in Yarrowia lipolytica var. indica. Arch Microbiol 196:545-556. https://doi.org/10.1007/s00203-014-0990-2
Papanikolaou S, Chevalot I, Galiotou-Panayotou M, et al (2007) Industrial derivative of tallow:a promising renewable substrate for microbial lipid, single-cell protein and lipase production by Yarrowia lipolytica. Electron J Biotechnol 10:0-0. https://doi.org/10.2225/vol10-issue3-fulltext-8
Papanikolaou S, Galiotou-Panayotou M, Fakas S et al (2008) Citric acid production by Yarrowia lipolytica cultivated on olive-mill wastewater-based media. Bioresour Technol 99:2419-2428. https://doi.org/10.1016/j.biortech.2007.05.005
Park CS, Chang CC, Ryu DDY (2000) Expression and high-level secretion of Trichoderma reesei Endoglucanase I in Yarrowia lipolytica. Appl Biochem Biotechnol 87:1-16. https://doi. org/10.1385/ABAB:87:1
Park J-N, Song Y, Kim J-Y, et al (2008) A novel YlMPO1 gene derived from Yarrowia lipolytica and a process for preparing a glycoprotein not being mannosylphosphorylated by using a mutated Yarrowia lipolytica in which YlMPO1 gene is disrupted. World patent application, WO2008136564 A1
Park Y-K, Korpys P, Kubiak M, et al (2019) Engineering the architecture of erythritol-inducible promoters for regulated and enhanced gene expression in Yarrowia lipolytica. FEMS Yeast Res 19(1). https://doi.org/10.1093/femsyr/foy105
Pérez-Campo FM, Domínguez A (2001) Factors affecting the morphogenetic switch in Yarrowia lipolytica. Curr Microbiol 43:429-433. https://doi.org/10.1007/s002840010333
Roth R, Moodley V, van Zyl P (2009) Heterologous expression and optimized production of an Aspergillus aculeatus Endo-1,4-β-mannanase in Yarrowia lipolytica. Mol Biotechnol 43:112-120. https://doi.org/10.1007/s12033-009-9187-3
Ruiz-Herrera J, Sentandreu R (2002) Different effectors of dimorphism in Yarrowia lipolytica. Arch Microbiol 178:477-483. https://doi.org/10.1007/s00203-002-0478-3
Sassi H, Delvigne F, Kar T et al (2016) Deciphering how LIP2 and POX2 promoters can optimally regulate recombinant protein production in the yeast Yarrowia lipolytica. Microb Cell Factories 15(1):159. https://doi.org/10.1186/s12934-016-0558-8
Sassi H, Delvigne F, Kallel H, Fickers P (2017) pH and not cell morphology modulate pLIP2 induction in the dimorphic yeast Yarrowia lipolytica. Curr Microbiol 74:413-417. https://doi. org/10.1007/s00284-017-1207-0
Shabbir Hussain M, Gambill L, Smith S, Blenner MA (2016) Engineering promoter architecture in oleaginous yeast Yarrowia lipolytica. ACS Synth Biol 5:213-223. https://doi.org/10.1021/acssynbio.5b00100
Song Y, Choi MH, Park J-N et al (2007) Engineering of the yeast Yarrowia lipolytica for the production of glycoproteins lacking the outer-chain mannose residues of N-glycans. Appl Environ Microbiol 73:4446-4454. https://doi.org/10.1128/AEM.02058-06
Spagnuolo M, Shabbir Hussain M, Gambill L, Blenner M (2018) Alternative Substrate Metabolism in Yarrowia lipolytica. Front Microbiol 9:1077. https://doi.org/10.3389/fmicb.2018.01077
Szabo R (2001) Cla4 protein kinase is essential for filament formation and invasive growth of Yarrowia lipolytica. Mol Genet Genomics 265:172-179. https://doi.org/10.1007/s004380000405
Tharaud C, Ribet A-M, Costes C, Gaillardin C (1992) Secretion of human blood coagulation factor XIIIa by the yeast Yarrowia lipolytica. Gene 121:111-119. https://doi. org/10.1016/0378-1119(92)90168-O
Theron CW, Berrios J, Delvigne F, Fickers P (2018) Integrating metabolic modeling and population heterogeneity analysis into optimizing recombinant protein production by Komagataella (Pichia) pastoris. Appl Microbiol Biotechnol 102:63-80. https://doi.org/10.1007/s00253-017-8612-y
Tiels P, Baranova E, Piens K et al (2012) A bacterial glycosidase enables mannose-6-phosphate modification and improved cellular uptake of yeast-produced recombinant human lysosomal enzymes. Nat Biotechnol 30:1225-1231. https://doi.org/10.1038/nbt.2427
Timoumi A, Cléret M, Bideaux C et al (2017a) Dynamic behavior of Yarrowia lipolytica in response to pH perturbations: dependence of the stress response on the culture mode. Appl Microbiol Biotechnol 101:351-366. https://doi.org/10.1007/s00253-016-7856-2
Timoumi A, Bideaux C, Guillouet SE et al (2017b) Influence of oxygen availability on the metabolism and morphology of Yarrowia lipolytica: insights into the impact of glucose levels on dimorphism. Appl Microbiol Biotechnol 101:7317-7333. https://doi.org/10.1007/s00253-017-8446-7
Timoumi A, Guillouet SE, Molina-Jouve C et al (2018) Impacts of environmental conditions on product formation and morphology of Yarrowia lipolytica. Appl Microbiol Biotechnol 102:3831-3848. https://doi.org/10.1007/s00253-018-8870-3
Torres-Guzman JC, Domínguez A (1997) HOY1, a homeo gene required for hyphal formation in Yarrowia lipolytica. Mol Cell Biol 17:6283-6293
Trassaert M, Vandermies M, Carly F et al (2017) New inducible promoter for gene expression and synthetic biology in Yarrowia lipolytica. Microb Cell Factories 16(1):141. https://doi. org/10.1186/s12934-017-0755-0
United Nations Framework Convention on Climate Change (2008) Kyoto protocol reference manual on accounting of emissions and assigned amounts. https://unfccc.int/resource/docs/publications/08_unfccc_kp_ref_manual.pdf.
van Rensburg E, den Haan R, Smith J et al (2012) The metabolic burden of cellulase expression by recombinant Saccharomyces cerevisiae Y294 in aerobic batch culture. Appl Microbiol Biotechnol 96:197-209. https://doi.org/10.1007/s00253-012-4037-9
van Zyl PJ (2011) A method for producing a polypeptide in Yarrowia lipolytica. World patent application, WO2011148339 A1
Vandermies M, Kar T, Carly F et al (2018) Yarrowia lipolytica morphological mutant enables lasting in situ immobilization in bioreactor. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-018-9006-5
Verbeke J, Beopoulos A, Nicaud J-M (2013) Efficient homologous recombination with short length flanking fragments in Ku70 deficient Yarrowia lipolytica strains. Biotechnol Lett 35:571-576. https://doi.org/10.1007/s10529-012-1107-0
Vieira Gomes AM, Souza Carmo T, Silva Carvalho L et al (2018) Comparison of yeasts as hosts for recombinant protein production. Microorganisms 6:38. https://doi.org/10.3390/microorganisms6020038
Walker C, Ryu S, Trinh CT (2018) Exceptional solvent tolerance in Yarrowia lipolytica Is enhanced by sterols. Metab Eng 54:83-95. https://doi.org/10.1101/324681
Wei S, Jian X, Chen J et al (2017) Reconstruction of genome-scale metabolic model of Yarrowia lipolytica and its application in overproduction of triacylglycerol. Bioresour Bioprocess 4:51. https://doi.org/10.1186/s40643-017-0180-6
Xie D (2017) Integrating Cellular and Bioprocess Engineering in the Non-Conventional Yeast Yarrowia lipolytica for Biodiesel Production: A Review. Front Bioeng Biotechnol 5:65. https:// doi.org/10.3389/fbioe.2017.00065
YaPing W, Ben R, Ling Z, Lixin M (2017) High-level expression of two thermophilic β-mannanases in Yarrowia lipolytica. Protein Expr Purif 133:1-7. https://doi.org/10.1016/j.pep.2017.02.008
Young TW, Wadeson A, Glover DJ et al (1996) The extracellular acid protease gene of Yarrowia lipolytica: sequence and pH-regulated transcription. Microbiology 142:2913-2921. https://doi. org/10.1099/13500872-142-10-2913
Zinjarde SS, Pant A, Deshpande MV (1998) Dimorphic transition in Yarrowia lipolytica isolated from oil-polluted sea water. Mycol Res 102:553-558. https://doi.org/10.1017/S0953756297005418