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Dynamic behavior of Yarrowia lipolytica in response to pH perturbations: dependence of the stress response on the culture mode

  • Applied microbial and cell physiology
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Abstract

Yarrowia lipolytica, a non-conventional yeast with a promising biotechnological potential, is able to undergo metabolic and morphological changes in response to environmental conditions. The effect of pH perturbations of different types (pulses, Heaviside) on the dynamic behavior of Y. lipolytica W29 strain was characterized under two modes of culture: batch and continuous. In batch cultures, different pH (4.5, 5.6 (optimal condition), and 7) were investigated in order to identify the pH inducing a stress response (metabolic and/or morphologic) in Y. lipolytica. Macroscopic behavior (kinetic parameters, yields, viability) of the yeast was slightly affected by pH. However, contrary to the culture at pH 5.6, a filamentous growth was induced in batch experiments at pH 4.5 and 7. Proportions of the filamentous subpopulation reached 84 and 93 % (v/v) under acidic and neutral conditions, respectively. Given the significant impact of neutral pH on morphology, pH perturbations from 5.6 to 7 were subsequently assayed in batch and continuous bioreactors. For both process modes, the growth dynamics remained fundamentally unaltered during exposure to stress. Nevertheless, morphological behavior of the yeast was dependent on the culture mode. Specifically, in batch bioreactors where cells proliferated at their maximum growth rate, mycelia were mainly formed. Whereas, in continuous cultures at controlled growth rates (from 0.03 to 0.20 h−1) even closed to the maximum growth rate of the stain (0.24 h−1), yeast-like forms predominated. This pointed out differences in the kinetic behavior of filamentous and yeast subpopulations, cell age distribution, and pH adaptive mechanisms between both modes of culture.

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References

  • Amanullah A, McFarlane CM, Emery AN, Nienow AW (2001) Scale-down model to simulate spatial pH variations in large-scale bioreactors. Biotechnol Bioeng 73:390–399. doi:10.1002/bit.1072

    Article  CAS  PubMed  Google Scholar 

  • Barth G, Gaillardin C (1996) Yarrowia lipolytica. In: Wolf K (ed) Nonconventional yeasts in biotechnology. Springer-Verlag, Berlin, pp. 313–388

    Chapter  Google Scholar 

  • Barth G, Gaillardin C (1997) Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev 19:219–237

    Article  CAS  PubMed  Google Scholar 

  • Bellou S, Makri A, Triantaphyllidou I-E, Papanikolaou S, Aggelis G (2014) Morphological and metabolic shifts of Yarrowia lipolytica induced by alteration of the dissolved oxygen concentration in the growth environment. Microbiol SGM 160:807–817. doi:10.1099/mic.0.074302-0

    Article  CAS  Google Scholar 

  • Bellou S, Triantaphyllidou IE, Aggeli D, Elazzazy AM, Baeshen MN, Aggelis G (2016) Microbial oils as food additives: recent approaches for improving microbial oil production and its polyunsaturated fatty acid content. Curr Opin Biotechnol 37:24–35. doi:10.1016/j.copbio.2015.09.005

    Article  CAS  PubMed  Google Scholar 

  • Botelho Nunes PM, da Rocha SM, Fonseca Amaral PF, Miguez d, Rocha-Leao MH (2013) Study of trans-trans farnesol effect on hyphae formation by Yarrowia lipolytica. Bioprocess Biosyst Eng 36:1967–1975. doi:10.1007/s00449-013-0973-8

    Article  Google Scholar 

  • Braga A, Mesquita DP, Amaral AL, Ferreira EC, Belo I (2016) Quantitative image analysis as a tool for Yarrowia lipolytica dimorphic growth evaluation in different culture media. J Biotechnol 217:22–30. doi:10.1016/j.jbiotec.2015.10.023

    Article  CAS  PubMed  Google Scholar 

  • Bussamara R, Fuentefria AM, de Oliveira ES, Broetto L, Simcikova M, Valente P, Schrank A, Vainstein MH (2010) Isolation of a lipase-secreting yeast for enzyme production in a pilot-plant scale batch fermentation. Bioresour Technol 101:268–275. doi:10.1016/j.biortech.2008.10.063

    Article  CAS  PubMed  Google Scholar 

  • Bylund F, Collet E, Enfors SO, Larsson G (1998) Substrate gradient formation in the large-scale bioreactor lowers cell yield and increases by-product formation. Bioprocess Eng 18:171–180. doi:10.1007/s004490050427

    Article  CAS  Google Scholar 

  • Cervantes-Chavez 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. doi:10.1111/j.1567-1364.2006.00084.x

    Article  CAS  PubMed  Google Scholar 

  • Cervantes-Chavez JA, Ruiz-Herrera J (2007) The regulatory subunit of protein kinase A promotes hyphal growth and plays an essential role in Yarrowia lipolytica. FEMS Yeast Res 7:929–940. doi:10.1111/j.1567-1364.2007.00265.x

    Article  CAS  PubMed  Google Scholar 

  • Cervantes-Chavez 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. doi:10.1016/j.fgb.2009.02.005

    Article  CAS  PubMed  Google Scholar 

  • Coelho MAZ, Amaral PFF, Belo I (2010) Yarrowia lipolytica: an industrial workhorse. In: Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology Advances, pp. 930–940

  • Deak T (2001) Identification of yeasts isolated from poultry meat. Acta Biol Hung 52:195–200. doi:10.1556/ABiol.52.2001.2-3.3

    Article  CAS  PubMed  Google Scholar 

  • Deive FJ, Angeles Sanroman M, Longo MA (2010) A comprehensive study of lipase production by Yarrowila lipolytica CECT 1240 (ATCC 18942): from shake flask to continuous bioreactor. J Chem Technol Biotechnol 85:258–266. doi:10.1002/jctb.2301

    Article  CAS  Google Scholar 

  • Delvigne F, Goffin P (2014) Microbial heterogeneity affects bioprocess robustness: dynamic single-cell analysis contributes to understanding of microbial populations. Biotechnol J 9:61–72. doi:10.1002/biot.201300119

    Article  CAS  PubMed  Google Scholar 

  • Delvigne F, Boxus M, Ingels S, Thonart P (2009) Bioreactor mixing efficiency modulates the activity of a prpoS::GFP reporter gene in E. coli. Microb Cell Fact 8 doi:10.1186/1475–2859–8-15

  • Enfors SO, Jahic M, Rozkov A, Xu B, Hecker M, Jurgen B, Kruger E, Schweder T, Hamer G, O’Beirne D, Noisommit-Rizzi N, Reuss M, Boone L, Hewitt C, McFarlane C, Nienow A, Kovacs T, Tragardh C, Fuchs L, Revstedt J, Friberg PC, Hjertager B, Blomsten G, Skogman H, Hjort S, Hoeks F, Lin HY, Neubauer P, van der Lans R, Luyben K, Vrabel P, Manelius A (2001) Physiological responses to mixing in large scale bioreactors. J Biotechnol 85:175–185. doi:10.1016/s0168-1656(00)00365-5

    Article  CAS  PubMed  Google Scholar 

  • Enshaeieh M, Abdoli A, Nahvi I (2013) Medium optimization for biotechnological production of single cell oil using Candida gali and Yarrowia lipolytica M7. J Cell Mol Res 5:17–23

    Google Scholar 

  • Fickers P, Benetti PH, Wache Y, Marty A, Mauersberger S, Smit MS, Nicaud JM (2005) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:527–543. doi:10.1016/j.femsyr.2004.09.004

    Article  CAS  PubMed  Google Scholar 

  • Fickers P, Destain J, Thonart P (2009) Improvement of Yarrowia lipolytica lipase production by fed-batch fermentation. J Basic Microbiol 49:212–215. doi:10.1002/jobm.200800186

    Article  CAS  PubMed  Google Scholar 

  • Finogenova TV, Kamzolova SV, Dedyukhina EG, Shishkanova NV, Il’chenko AP, Morgunov IG, Chernyavskaya OG, Sokolov AP (2002) Biosynthesis of citric and isocitric acids from ethanol by mutant Yarrowia lipolytica N 1 under continuous cultivation. Appl Microbiol Biotechnol 59:493–500. doi:10.1007/s00253-002-1022-8

    Article  CAS  PubMed  Google Scholar 

  • Galvagno MA, Iannone LJ, Bianchi J, Kronberg F, Rost E, Carstens MR, Cerrutti P (2011) Optimization of biomass production of a mutant of Yarrowia lipolytica with an increased lipase activity using raw glycerol. Rev Argent Microbiol 43:218–225

    CAS  PubMed  Google Scholar 

  • Gasmi N, Ayed A, Nicaud J-M, Kallel H (2011) Design of an efficient medium for heterologous protein production in Yarrowia lipolytica: case of human interferon alpha 2b. Microb Cell Factories 10. doi:10.1186/1475-2859-10-38

  • Goncalves FAG, Colen G, Takahashi JA (2014) Yarrowia lipolytica and its multiple applications in the biotechnological industry. Sci World J. doi:10.1155/2014/476207

    Google Scholar 

  • Gonzalez-Lopez CI, Ortiz-Castellanos L, Ruiz-Herrera J (2006) The ambient pH response rim pathway in Yarrowia lipolytica: identification of YlRIM9 and characterization of its role in dimorphism. Curr Microbiol 53:8–12. doi:10.1007/s00284-005-0070-6

    Article  CAS  PubMed  Google Scholar 

  • Guevaraolvera L, Calvomendez C, Ruizherrera J (1993) The role of polyamine metabolism in dimorphism of Yarrowia lipolytica. J Gen Microbiol 139:485–493

    Article  CAS  Google Scholar 

  • Han S, Delvigne F, Brognaux A, Charbon GE, Sorensen SJ (2013) Design of growth-dependent biosensors based on destabilized GFP for the detection of physiological behavior of Escherichia coli in heterogeneous bioreactors. Biotechnol Prog 29:553–563. doi:10.1002/btpr.1694

    Article  CAS  PubMed  Google Scholar 

  • Hurtado CAR, Beckerich JM, Gaillardin C, Rachubinski RA (2000) A Rac homolog is required for induction of hyphal growth in the dimorphic yeast Yarrowia lipolytica. J Bacterio l 182:2376–2386. doi:10.1128/jb.182.9.2376-2386.2000

    Article  CAS  Google Scholar 

  • Jazini M, Cekici G, Herwig C (2014) Quantifying the effects of frequency and amplitude of periodic oxygen-related stress on recombinant protein production in Pichia pastoris. Bioengineering:47–61

  • Kar T, Delvigne F, Masson M, Destain J, Thonart P (2008) Investigation of the effect of different extracellular factors on the lipase production by Yarrowia lipolityca on the basis of a scale-down approach. J Ind Microbiol Biotechnol 35:1053–1059. doi:10.1007/s10295-008-0382-1

    Article  CAS  PubMed  Google Scholar 

  • 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 Envir 15:585–595

    Google Scholar 

  • Kawasse FM, Amaral PF, Rocha-Leao MHM, Amaral AL, Ferreira EC, Coelho MAZ (2003) Morphological analysis of Yarrowia lipolytica under stress conditions through image processing. Bioprocess Biosyst Eng 25:371–375. doi:10.1007/s00449-003-0319-z

    Article  CAS  PubMed  Google Scholar 

  • Kraiem H, Ben Gaïda L, Manon Y, Anne-Archard D, Fillaudeau L (2013) Impact of cell physiology and densities during oxidative axenic cultures of Yarrowia lipolytica on physico-chemical properties of broth. In: 9th World Congress of Chemical Engineering, 18–23 August 2013 (Seoul, Korea, Republic Of)

  • Lara AR, Galindo E, Ramirez OT, Palomares LA (2006) Living with heterogeneities in bioreactors. Mol Biotechnol 34:355–381. doi:10.1385/mb:34:3:355

    Article  CAS  PubMed  Google Scholar 

  • Levinson WE, Kurtzman CP, Kuo TM (2007) Characterization of Yarrowia lipolytica and related species for citric acid production from glycerol. Enzym Microb Technol 41:292–295. doi:10.1016/j.enzmictec.2007.02.005

    Article  CAS  Google Scholar 

  • Lim JS, Kim JH, Kim C, Kim SW (2002) Morphological and rheological properties of culture broth of Cephalosporium acremonium M25. Korea Aust Rheol J 14:11–16

    Google Scholar 

  • Lopes M, Gomes N, Goncalves C, Coelho MAZ, Mota M, Belo I (2008) Yarrowia lipolytica lipase production enhanced by increased air pressure. Lett Appl Microbiol 46:255–260. doi:10.1111/j.1472-765X.2007.02299.x

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s12010-008-8359-0

    Article  CAS  PubMed  Google Scholar 

  • Madzak C, Gaillardin C, Beckerich JM (2004) Heterologous protein expression and secretion in the non-conventional yeast Yarrowia lipolytica: a review. J Biotechnol 109:63–81. doi:10.1016/j.jbiotec.2003.10.027

    Article  CAS  PubMed  Google Scholar 

  • Madzak C, Otterbein L, Chamkha M, Moukha S, Asther M, Gaillardin C, Beckerich JM (2005) Heterologous production of a laccase from the basidiomycete Pycnoporus cinnabarinus in the dimorphic yeast Yarrowia lipolytica. FEMS Yeast Res 5:635–646. doi:10.1016/j.femsyr.2004.10.009

    Article  CAS  PubMed  Google Scholar 

  • Makri A, Fakas S, Aggelis G (2010) Metabolic activities of biotechnological interest in Yarrowia lipolytica grown on glycerol in repeated batch cultures. Bioresour Technol 101:2351–2358. doi:10.1016/j.biortech.2009.11.024

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Vazquez A, Gonzalez-Hernandez A, Dominguez A, Rachubinski R, Riquelme M, Cuellar-Mata P, Torres Guzman JC (2013) Identification of the transcription factor Znc1p, which regulates the yeast-to-hypha transition in the dimorphic yeast Yarrowia lipolytica. PLoS One 8 doi:10.1371/journal.pone.0066790

  • McIlvaine TC (1921) A buffer solution for colorimetric comparison. J Biol Chem 49:183–186

    CAS  Google Scholar 

  • Morin M, Monteoliva L, Insenser M, Gil C, Dominguez A (2007) Proteomic analysis reveals metabolic changes during yeast to hypha transition in Yarrowia lipolytica. J Mass Spectrom 42:1453–1462. doi:10.1002/jms.1284

    Article  CAS  PubMed  Google Scholar 

  • Novotny C, Dolezalova L, Lieblova J (1994) Dimorphic growth and lipase production in lipolytic yeasts. Folia Microbiol 39:71–73. doi:10.1007/bf02814534

    Article  CAS  Google Scholar 

  • Ochoa-Estopier A, Guillouet SE (2014) D-stat culture for studying the metabolic shifts from oxidative metabolism to lipid accumulation and citric acid production in Yarrowia lipolytica. J Biotechnol 170:35–41. doi:10.1016/j.jbiotec.2013.11.008

    Article  CAS  PubMed  Google Scholar 

  • O’Shea DG, Walsh PK (2000) The effect of culture conditions on the morphology of the dimorphic yeast Kluyveromyces marxianus var. marxianus NRRLy2415: a study incorporating image analysis. Appl Microbiol Biotechnol 53:316–322

    Article  PubMed  Google Scholar 

  • Ota Y, Oikawa S, Morimoto Y, Minoda Y (1984) Nutritional factors causing mycelial development of Saccharomycopsis lipolytica. Agric Biol Chem 48:1933–1939

    CAS  Google Scholar 

  • Palande AS, Kulkarni SV, Leon-Ramirez C, Campos-Gongora E, Ruiz-Herrera J, Deshpande MV (2014) Dimorphism and hydrocarbon metabolism in Yarrowia lipolytica var. indica. Arch Microbiol 196:545–556. doi:10.1007/s00203-014-0990-2

    Article  CAS  PubMed  Google Scholar 

  • Papanikolaou S, Aggelis G (2009) Biotechnological valorization of biodiesel derived glycerol waste through production of single cell oil and citric acid by Yarrowia lipolytica. Lipid Technol 21:83–87

    Article  CAS  Google Scholar 

  • Papanikolaou S, Galiotou-Panayotou M, Chevalot I, Komaitis M, Marc I, Aggelis G (2006) Influence of glucose and saturated free-fatty acid mixtures on citric acid and lipid production by Yarrowia lipolytica. Curr Microbiol 52:134–142. doi:10.1007/s00284-005-0223-7

    Article  CAS  PubMed  Google Scholar 

  • Papanikolaou S, Chevalot I, Galiotou-Panayotou M, Komaitis M, Marc I, Aggelis G (2007) Industrial derivative of tallow: a promising renewable substrate for microbial lipid, single-cell protein and lipase production by Yarrowia lipolytica. Electron J Biotechnol 10:425–435. doi:10.2225/vol10-issue3-fulltext-8

    Article  CAS  Google Scholar 

  • Parfene G, Horincar V, Tyagi AK, Malik A, Bahrim G (2013) Production of medium chain saturated fatty acids with enhanced antimicrobial activity from crude coconut fat by solid state cultivation of Yarrowia lipolytica. Food Chem 136:1345–1349. doi:10.1016/j.foodchem.2012.09.057

    Article  CAS  PubMed  Google Scholar 

  • Perez-Campo FM, Dominguez A (2001) Factors affecting the morphogenetic switch in Yarrowia lipolytica. Curr Microbiol 43:429–433. doi:10.1007/s002840010333

    Article  CAS  PubMed  Google Scholar 

  • Rakicka M, Lazar Z, Dulermo T, Fickers P, Nicaud JM (2015) Lipid production by the oleaginous yeast Yarrowia lipolytica using industrial by-products under different culture conditions. Biotechnol Biofuels 8 doi:10.1186/s13068-015-0286-z

  • Robak M, Boruczkowski T, Drozdz W, Lazar Z, Baranowska M, Przado D, Steininger M (2011) Application of the yeasts Yarrowia lipolytica for in-situ bioremediation of soil contaminated with creosote oil a case study. OCHR SR 33:27–33

    Google Scholar 

  • Rodriguez C, Dominguez A (1984) The growth characteristics of Saccharomycopsis lipolytica: morphology and induction of mycelium formation. Can J Microbiol 30:605–612

    Article  CAS  Google Scholar 

  • Ron EZ, Rosenberg E (2002) Biosurfactants and oil bioremediation. Curr Opin Biotechnol 13:249–252. doi:10.1016/s0958-1669(02)00316-6

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Herrera J, Sentandreu R (2002) Different effectors of dimorphism in Yarrowia lipolytica. Arch Microbiol 178:477–483. doi:10.1007/s00203-002-0478-3

    Article  CAS  PubMed  Google Scholar 

  • Rymowicz W, Rywinska A, Zarowska B, Juszczyk P (2006) Citric acid production from raw glycerol by acetate mutants of Yarrowia lipolytica. Chem Pap-Chem Zvesti 60:391–394. doi:10.2478/s11696-006-0071-3

    CAS  Google Scholar 

  • Rywinska A, Juszczyk P, Wojtatowicz M, Rymowicz W (2011) Chemostat study of citric acid production from glycerol by Yarrowia lipolytica. J Biotechnol 152:54–57. doi:10.1016/j.jbiotec.2011.01.007

    Article  CAS  PubMed  Google Scholar 

  • Sarris D, Galiotou-Panayotou M, Koutinas AA, Komaitis M, Papanikolaou S (2011) Citric acid, biomass and cellular lipid production by Yarrowia lipolytica strains cultivated on olive mill wastewater-based media. J Chem Technol Biotechnol 86:1439–1448. doi:10.1002/jctb.2658

    Article  CAS  Google Scholar 

  • Sauer M, Porro D, Mattanovich D, Branduardi P (2008) Microbial production of organic acids: expanding the markets. Trends Biotechnol 26:100–108. doi:10.1016/j.tibtech.2007.11.006

    Article  CAS  PubMed  Google Scholar 

  • Schrickx JM, Krave AS, Verdoes JC, Vandenhondel C, Stouthamer AH, Vanverseveld HW (1993) Growth and product formation in chemostat and recycling cultures by Aspergillus niger N402 and a glucoamylase overproducing transformant, provided with multiple copies of the glaA gene. J Gen Microbiol 139:2801–2810

    Article  CAS  PubMed  Google Scholar 

  • Sekova VY, Gessler NN, Isakova EP, Antipov AN, Dergacheva DI, Deryabina YI, Trubnikova EV (2015) Redox status of extremophilic yeast Yarrowia lipolytica during adaptation to pH-stress. Appl Biochem Microbiol 51:649–654. doi:10.1134/s0003683815060137

    Article  CAS  Google Scholar 

  • Shepherd MG, Sullivan PA (1976) The production and growth characteristics of yeast and mycelial forms of Candida albicans in continuous culture. J Gen Microbiol 93:361–370

    Article  CAS  PubMed  Google Scholar 

  • Sunya S, Delvigne F, Uribelarrea JL, Molina-Jouve C, Gorret N (2012) Comparison of the transient responses of Escherichia coli to a glucose pulse of various intensities. Appl Microbiol Biotechnol 95:1021–1034. doi:10.1007/s00253-012-3938-y

    Article  CAS  PubMed  Google Scholar 

  • Topiltin Morales-Vargas A, Dominguez A, Ruiz-Herrera J (2012) Identification of dimorphism-involved genes of Yarrowia lipolytica by means of microarray analysis. Res Microbiol 163:378–387. doi:10.1016/j.resmic.2012.03.002

    Article  PubMed  Google Scholar 

  • Walker GM, Oneill JD (1990) Morphological and metabolic changes in the yeast Kluyveromyces marxianus var. marxianus NRRLy2415 during fermentation of lactose. J Chem Technol Biotechnol 49:75–89

    Article  CAS  Google Scholar 

  • Wiebe MG, Trinci APJ (1991) Dilution rate as a determinant of mycelial morphology in continuous culture. Biotechnol Bioeng 38:75–81. doi:10.1002/bit.260380110

    Article  CAS  PubMed  Google Scholar 

  • Workman M, Holt P, Thykaer J (2013) Comparing cellular performance of Yarrowia lipolytica during growth on glucose and glycerol in submerged cultivations. AMB Express 3 doi:10.1186/2191–0855–3-58

  • Wucherpfennig T, Kiep KA, Driouch H, Wittmann C, Krull R (2010) Morphology and rheology in filamentous cultivations. In: Laskin AI, Sariaslani S, Gadd GM (eds). Adv Appl Microbiol 72:89–136. doi:10.1016/s0065-2164(10)72004-9

  • Yalcin HT, Ucar FB (2009) Isolation and characterization of cheese spoiler yeast isolated from Turkish white cheeses. Ann Microbiol 59:477–483

    Article  CAS  Google Scholar 

  • Zinjarde SS, Pant A, Deshpande MV (1998) Dimorphic transition in Yarrowia lipolytica isolated from oil-polluted sea water. Mycol Res 102:553–558. doi:10.1017/s0953756297005418

    Article  Google Scholar 

  • Zinjarde SS, Kale BV, Vishwasrao PV, Kumar AR (2008) Morphogenetic behavior of tropical marine yeast Yarrowia lipolytica in response to hydrophobic substrates. J Microbiol Biotechnol 18:1522–1528

    CAS  PubMed  Google Scholar 

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Acknowledgments

Financial support for this study was provided by Airbus, Agence Nationale de la Recherche (ANR), and Commissariat aux Investissements d’Avenir via the project ProBio3 “Biocatalytic production of lipidic bioproducts from renewable resources and industrial by-products: BioJet Fuel Application” (ref. ANR-11-BTBT-0003).

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  1. LISBP, Université de Toulouse, CNRS, INRA, INSA, Toulouse, France

    Asma Timoumi, Mégane Cléret, Carine Bideaux, Stéphane E. Guillouet, Carole Molina-Jouve, Luc Fillaudeau & Nathalie Gorret

  2. Airbus Operations S.A.S, 316 Route de Bayonne, 31060, Toulouse, France

    Yohan Allouche

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Timoumi, A., Cléret, M., Bideaux, C. et al. 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 (2017). https://doi.org/10.1007/s00253-016-7856-2

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