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Citric Acid Production by Yarrowia lipolytica

Abstract

Recently, with an increasing annual demand of more than two million tons, citric acid (CA) has become the main additive and functional component in the food, pharmaceutical, and chemical industries. This rising demand has induced research to search for alternative and cheap ways to fulfil CA requirements in industry. Lately, Yarrowia lipolytica has been considered as a promising microorganism in the production of CA since it has many advantages over moulds: mainly high productivity, easier cultivation (convenient for continuous process), and the capability to use a wide range of agricultural or industrial by-products and wastes as cheap carbon sources. CA production by this yeast depends on certain factors such as medium composition (type and concentrations of carbon, nitrogen, and trace elements) and the type of strain used (wild, mutant, or genetically engineered), as well as cultivation conditions (pH, temperature, dissolved oxygen, etc.). This review principally details recent studies concerning CA production by Y. lipolytica with an emphasis on techniques to increase productivity and yield to meet the expanding demand for this organic acid. Suitable substrates and production factors for high and cost-efficient CA production are discussed. Downstream processes and production systems are also reviewed.

Keywords

  • Yeast
  • Yarrowia lipolytica
  • Citric acid
  • Citric acid biosynthesis
  • Factors

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Fig. 4.1

References

  • Abghari A, Chen S (2017) Engineering Yarrowia lipolytica for enhanced production of lipid and citric acid. Fermentation 3(3):34

    CrossRef  CAS  Google Scholar 

  • Amaral PFF, Lehocky M, Barros-Timmons AMV, Rocha-Leao MHM, Coelho MAZ, Coutinho JAP (2006) Cell surface characterization of Yarrowia lipolytica IMUFRJ 50682. Yeast 23(12):867–877

    CAS  PubMed  CrossRef  Google Scholar 

  • Anastassiadis S, Rehm HJ (2005) Continuous citric acid secretion by a high specific pH dependent active transport system in yeast Candida oleophila ATCC 20177. Electron J Biotechnol 8(2):146–161

    CAS  CrossRef  Google Scholar 

  • Anastassiadis S, Rehm HJ (2006) Citric acid production from glucose by yeast Candida oleophila ATCC 20177 under batch, continuous and repeated batch cultivation. Electron J Biotechnol 9(1):26–39

    CAS  CrossRef  Google Scholar 

  • Anastassiadis S, Aivasidis A, Wandrey C (2002) Citric acid production by Candida strains under intracellular nitrogen limitation. Appl Microbiol Biotechnol 60(1–2):81–87

    CAS  PubMed  Google Scholar 

  • Anastassiadis S, Morgunov IG, Kamzolova SV, Finogenova TV (2008) Citric acid production patent review. Recent Pat Biotechnol 2(2):107–123

    CAS  PubMed  CrossRef  Google Scholar 

  • Angumeenal AR, Venkappayya D (2013) An overview of citric acid production. Lwt-Food Sci Technol 50(2):367–370

    CAS  CrossRef  Google Scholar 

  • Antonucci S, Bravi M, Bubbico R, Di Michele A, Verdone N (2001) Selectivity in citric acid production by Yarrowia lipolytica. Enzym Microb Technol 28(2–3):189–195

    CAS  CrossRef  Google Scholar 

  • Apelblat A (2014) Citric acid. Springer, Cham

    CrossRef  Google Scholar 

  • Arslan NP, Aydogan MN, Taskin M (2016) Citric acid production from partly deproteinized whey under non-sterile culture conditions using immobilized cells of lactose positive and cold-adapted Yarrowia lipolytica B9. J Biotechnol 231:32–39

    CAS  PubMed  CrossRef  Google Scholar 

  • Arzumanov TE, Shishkanova NV, Finogenova TV (2000) Biosynthesis of citric acid by Yarrowia lipolytica repeat-batch culture on ethanol. Appl Microbiol Biotechnol 53(5):525–529

    CAS  PubMed  CrossRef  Google Scholar 

  • Athenaki M, Gardeli C, Diamantopoulou P, Tchakouteu SS, Sarris D, Philippoussis A, Papanikolaou S (2018) Lipids from yeasts and fungi: physiology, production and analytical considerations. J Appl Microbiol 124(2):336–367

    CAS  PubMed  CrossRef  Google Scholar 

  • Barth G, Gaillardin C (1997) Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev 19(4):219–237

    CAS  PubMed  CrossRef  Google Scholar 

  • Bellou S, Makri A, Triantaphyllidou IE, Papanikolaou S, Aggelis G (2014) Morphological and metabolic shifts of Yarrowia lipolytica induced by alteration of the dissolved oxygen concentration in the growth environment. Microbiology-Sgm 160:807–817

    CAS  CrossRef  Google Scholar 

  • Carsanba E, Papanikolaou S, Erten H (2018) Production of oils and fats by oleaginous microorganisms with an emphasis given to the potential of the nonconventional yeast Yarrowia lipolytica. Crit Rev Biotechnol 38(8):1230–1243

    CAS  PubMed  CrossRef  Google Scholar 

  • Cavallo E, Charreau H, Cerrutti P, Foresti ML (2017) Yarrowia lipolytica: a model yeast for citric acid production. FEMS Yeast Res 17(8)

    Google Scholar 

  • Chatzifragkou A, Makri A, Belka A, Bellou S, Mavrou M, Mastoridou M, Mystrioti P, Onjaro G, Aggelis G, Papanikolaou S (2011) Biotechnological conversions of biodiesel derived waste glycerol by yeast and fungal species. Energy 36(2):1097–1108

    CAS  CrossRef  Google Scholar 

  • Ciriminna R, Meneguzzo F, Delisi R, Pagliaro M (2017) Citric acid: emerging applications of key biotechnology industrial product. Chem Cent J 11:22

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Coelho MAZ, Amaral P, Belo I (2010) Yarrowia lipolytica: an industrial workhorse. Appl Microbiol Microb Biotechnol 2:930–944

    Google Scholar 

  • Crolla A, Kennedy KJ (2001) Optimization of citric acid production from Candida lipolytica Y-1095 using n-paraffin. J Biotechnol 89(1):27–40

    CAS  PubMed  CrossRef  Google Scholar 

  • Crolla A, Kennedy K (2004a) In-line mixing for production of citric acid by Candida lipolytica grown on n-paraffins. J Chem Technol Biotechnol 79(7):720–728

    CAS  CrossRef  Google Scholar 

  • Crolla A, Kennedy KJ (2004b) Fed-batch production of citric acid by Candida lipolytica grown on n-paraffins. J Biotechnol 110(1):73–84

    CAS  PubMed  CrossRef  Google Scholar 

  • Darvishi F, Nahvi I, Zarkesh-Esfahani H, Momenbeik F (2009) Effect of plant oils upon lipase and citric acid production in Yarrowia lipolytica yeast. J Biomed Biotechnol 7

    Google Scholar 

  • Dhillon GS, Brar SK, Verma M, Tyagi RD (2011) Recent advances in citric acid bio-production and recovery. Food Bioprocess Technol 4(4):505–529

    CAS  CrossRef  Google Scholar 

  • Dourou M, Kancelista A, Juszczyk P, Sarris D, Bellou S, Triantaphyllidou IE, Rywinska A, Papanikolaou S, Aggelis G (2016) Bioconversion of olive mill wastewater into high-added value products. J Clean Prod 139:957–969

    CAS  CrossRef  Google Scholar 

  • Egermeier M, Russmayer H, Sauer M, Marx H (2017) Metabolic flexibility of Yarrowia lipolytica growing on glycerol. Front Microbiol 8:49–49

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Ferreira P, Lopes M, Mota M, Belo I (2016a) Oxygen mass transfer impact on citric acid production by Yarrowia lipolytica from crude glycerol. Biochem Eng J 110:35–42

    CAS  CrossRef  Google Scholar 

  • Ferreira P, Lopes M, Mota M, Belo I (2016b) Oxygen transfer rate and pH as major operating parameters of citric acid production from glycerol by Yarrowia lipolytica W29 and CBS 2073. Chem Pap 70(7):869–876

    CAS  CrossRef  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(6–7):527–543

    CAS  PubMed  CrossRef  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(4–5):493–500

    CAS  PubMed  Google Scholar 

  • Fontanille P, Kumar V, Christophe G, Nouaille R, Larroche C (2012) Bioconversion of volatile fatty acids into lipids by the oleaginous yeast Yarrowia lipolytica. Bioresour Technol 114:443–449

    CAS  PubMed  CrossRef  Google Scholar 

  • Forster A, Jacobs K, Juretzek T, Mauersberger S, Barth G (2007) Overexpression of the ICL1 gene changes the product ratio of citric acid production by Yarrowia lipolytica. Appl Microbiol Biotechnol 77(4):861–869

    PubMed  CrossRef  CAS  Google Scholar 

  • Fu G-Y, Lu Y, Chi Z, Liu G-L, Zhao S-F, Jiang H, Chi Z-M (2016) Cloning and characterization of a pyruvate carboxylase gene from Penicillium rubens and overexpression of the genein the yeast Yarrowia lipolytica for Enhanced Citric Acid Production. Mar Biotechnol 18(1):1–14

    CAS  CrossRef  Google Scholar 

  • Gaden EL (2000) Fermentation process kinetics (reprinted from J of biochemical and microbiological technology and engineering, vol 1, pg 413, 1959). Biotechnol Bioeng 67(6):629–635

    PubMed  CrossRef  Google Scholar 

  • Goncalves FAG, Colen G, Takahashi JA (2014) Yarrowia lipolytica and its multiple applications in the biotechnological industry. Sci World J 14

    Google Scholar 

  • Grewal HS, Kalra KL (1995) Fungal production of citric-acid. Biotechnol Adv 13(2):209–234

    CAS  PubMed  CrossRef  Google Scholar 

  • Hamissa FA, Abouzeid AZA, Redwan AA (1981) Fermentative production of citric-acid by yeasts. Agricult Wastes 3(1):21–33

    CAS  CrossRef  Google Scholar 

  • Holz M, Forster A, Mauersberger S, Barth G (2009) Aconitase overexpression changes the product ratio of citric acid production by Yarrowia lipolytica. Appl Microbiol Biotechnol 81(6):1087–1096

    CAS  PubMed  CrossRef  Google Scholar 

  • Holz M, Otto C, Kretzschmar A, Yovkova V, Aurich A, Pötter M, Marx A, Barth G (2011) Overexpression of alpha-ketoglutarate dehydrogenase in Yarrowia lipolytica and its effect on production of organic acids. Appl Microbiol Biotechnol 89(5):1519–1526

    CAS  PubMed  CrossRef  Google Scholar 

  • Hou WL, Bao J (2018) Simultaneous saccharification and aerobic fermentation of high titer cellulosic citric acid by filamentous fungus Aspergillus niger. Bioresour Technol 253:72–78

    CAS  PubMed  CrossRef  Google Scholar 

  • Imandi SB, Bandaru VR, Somalanka SR, Garapati HR (2007) Optimization of medium constituents for the production of citric acid from byproduct glycerol using Doehlert experimental design. Enzym Microb Technol 40(5):1367–1372

    CAS  CrossRef  Google Scholar 

  • Imandi SB, Bandaru VVR, Somalanka SR, Bandaru SR, Garapati HR (2008) Application of statistical experimental designs for the optimization of medium constituents for the production of citric acid from pineapple waste. Bioresour Technol 99(10):4445–4450

    CAS  PubMed  CrossRef  Google Scholar 

  • Kamzolova SV, Morgunov IG (2017) Metabolic peculiarities of the citric acid overproduction from glucose in yeasts Yarrowia lipolytica. Bioresour Technol 243:433–440

    CAS  PubMed  CrossRef  Google Scholar 

  • Kamzolova SV, Shishkanova NV, Morgunov IG, Finogenova TV (2003) Oxygen requirements for growth and citric acid production of Yarrowia lipolytica. FEMS Yeast Res 3(2):217–222

    CAS  PubMed  CrossRef  Google Scholar 

  • Kamzolova SV, Morgunov IG, Aurich A, Perevoznikova OA, Shishkanova NV, Stottmeister U, Finogenova TV (2005) Lipase secretion and citric acid production in Yarrowia lipolytica yeast grown on animal and vegetable fat. Food Technol Biotechnol 43(2):113–122

    CAS  Google Scholar 

  • Kamzolova SV, Finogenova TV, Lunina YN, Perevoznikova OA, Minachova LN, Morgunov IG (2007) Characteristics of the growth on rapeseed oil and synthesis of citric and isocitric acids by Yarrowia lipolytica yeasts. Microbiology 76(1):20–24

    CAS  CrossRef  Google Scholar 

  • Kamzolova SV, Finogenova TV, Morgunov IG (2008) Microbiological production of citric and isocitric acids from sunflower oil. Food Technol Biotechnol 46(1):51–59

    CAS  Google Scholar 

  • Kamzolova SV, Lunina JN, Morgunov IG (2011) Biochemistry of citric acid production from rapeseed oil by Yarrowia lipolytica yeast. J Am Oil Chemists Soc 88(12):1965–1976

    CAS  CrossRef  Google Scholar 

  • Kamzolova SV, Lunina YN, Allayarov RK, Puntus IF, Laptev IA, Samoilenko VA, Morgunov IG (2015a) Biosynthesis of isocitric acid by the yeast Yarrowia lipolytica and its regulation. Appl Biochem Microbiol 51(2):249–254

    CAS  CrossRef  Google Scholar 

  • Kamzolova SV, Vinokurova NG, Lunina JN, Zelenkova NF, Morgunov IG (2015b) Production of technical-grade sodium citrate from glycerol-containing biodiesel waste by Yarrowia lipolytica. Bioresour Technol 193:250–255

    CAS  PubMed  CrossRef  Google Scholar 

  • Kautola H, Rymowicz W, Linko YY, Linko P (1991) Production of citric acid with immobilized Yarrowia lipolytica. Appl Microbiol Biotechnol 35(4):447–449

    CAS  CrossRef  Google Scholar 

  • Kieliszek M, Kot AM, Bzducha-Wrobel A, Blazejak S, Gientka I, Kurcz A (2017) Biotechnological use of Candida yeasts in the food industry: a review. Fungal Biol Rev 31(4):185–198

    CrossRef  Google Scholar 

  • Kubicek, C., Karaffa, L. 2001. Organic acids. in: Basic Biotechnology, Cambridge University Press Cambridge, pp. 305–315

    Google Scholar 

  • Kurtzman C, Fell JW (1998) The yeasts – a taxonomic study. Elsevier Science

    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(3):292–295

    CAS  CrossRef  Google Scholar 

  • Liu XY, Chi Z, Liu GL, Wang F, Madzak C, Chi ZM (2010) Inulin hydrolysis and citric acid production from inulin using the surface-engineered Yarrowia lipolytica displaying inulinase. Metab Eng 12(5):469–476

    CAS  PubMed  CrossRef  Google Scholar 

  • Liu XY, Lv JS, Xu JX, Zhang T, Deng YF, He JL (2015a) Citric acid production in Yarrowia lipolytica SWJ-1b yeast when grown on waste cooking oil. Appl Biochem Biotechnol 175(5):2347–2356

    CAS  PubMed  CrossRef  Google Scholar 

  • Liu XY, Lv JS, Zhang T, Deng YF (2015b) Citric acid production from hydrolysate of pretreated straw cellulose by Yarrowia lipolytica SWJ-1b using batch and fed-batch cultivation. Prep Biochem Biotechnol 45(8):825–835

    CAS  PubMed  CrossRef  Google Scholar 

  • Liu XY, Lv JS, Xu JX, Xia J, He AY, Zhang T, Li XQ, Xu JM (2018) Effects of osmotic pressure and pH on citric acid and erythritol production from waste cooking oil by Yarrowia lipolytica. Eng Life Sci 18(6):344–352

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Luo GS, Shan XY, Qi X, Lu YC (2004) Two-phase electro-electrodialysis for recovery and concentration of citric acid. Sep Purif Technol 38(3):265–271

    CrossRef  CAS  Google Scholar 

  • Luo HP, Cheng X, Liu GL, Zhou YJ, Lu YB, Zhang RD, Li X, Teng WK (2017) Citric acid production using a biological electrodialysis with bipolar membrane. J Membr Sci 523:122–128

    CAS  CrossRef  Google Scholar 

  • Madzak C (2015) Yarrowia lipolytica: recent achievements in heterologous protein expression and pathway engineering. Appl Microbiol Biotechnol 99(11):4559–4577

    CAS  PubMed  CrossRef  Google Scholar 

  • Magdouli S, Guedri T, Tarek R, Brar SK, Blais JF (2017) Valorization of raw glycerol and crustacean waste into value added products by Yarrowia lipolytica. Bioresour Technol 243:57–68

    CAS  PubMed  CrossRef  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(7):2351–2358

    CAS  PubMed  CrossRef  Google Scholar 

  • Mattey M (1992) The production of organic acids. Crit Rev Biotechnol 12(1–2):87–132

    CAS  PubMed  CrossRef  Google Scholar 

  • Max B, Salgado JM, Rodriguez N, Cortes S, Converti A, Dominguez JM (2010) Biotechnological production of citric acid. Braz J Microbiol 41(4):862–875

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Mitrea L, Trif M, Catoi AF, Vodnar DC (2017) Utilization of biodiesel derived glycerol for 1,3-PD and citric acid production. Microb Cell Factories 16:190

    CrossRef  CAS  Google Scholar 

  • Moeller L, Grunberg M, Zehnsdorf A, Strehlitz B, Bley T (2010) Biosensor online control of citric acid production from glucose by Yarrowia lipolytica using semicontinuous fermentation. Eng Life Sci 10(4):311–320

    CAS  CrossRef  Google Scholar 

  • Moeller L, Zehnsdorf A, Aurich A, Barth G, Bley T, Strehlitz B (2013) Citric acid production from sucrose by recombinant Yarrowia lipolytica using semicontinuous fermentation. Eng Life Sci 13(2):163–171

    CAS  CrossRef  Google Scholar 

  • Morgunov IG, Kamzolova SV, Lunina JN (2013) The citric acid production from raw glycerol by Yarrowia lipolytica yeast and its regulation. Appl Microbiol Biotechnol 97(16):7387–7397

    CAS  PubMed  CrossRef  Google Scholar 

  • Morgunov IG, Kamzolova SV, Dedyukhina EG, Chistyakova TI, Lunina JN, Mironov AA, Stepanova NN, Shemshura ON, Vainshtein MB (2017) Application of organic acids for plant protection against phytopathogens. Appl Microbiol Biotechnol 101(3):921–932

    CAS  PubMed  CrossRef  Google Scholar 

  • Nicaud JM (2012) Yarrowia lipolytica. Yeast 29(10):409–418

    CAS  PubMed  CrossRef  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

    CAS  PubMed  CrossRef  Google Scholar 

  • Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport and modeling. Biotechnol Adv 25(3):244–263

    CAS  PubMed  CrossRef  Google Scholar 

  • Papanikolaou S, Aggelis G (2002) Lipid production by Yarrowia lipolytica growing on industrial glycerol in a single-stage continuous culture. Bioresour Technol 82(1):43–49

    CAS  PubMed  CrossRef  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(4):83–87

    CAS  CrossRef  Google Scholar 

  • Papanikolaou S, Aggelis G (2010) Yarrowia lipolytica: a model microorganism used for the production of tailor-made lipids. Eur J Lipid Sci Technol 112(6):639–654

    CAS  CrossRef  Google Scholar 

  • Papanikolaou S, Aggelis G (2011) Lipids of oleaginous yeasts. Part I: biochemistry of single cell oil production. Eur J Lipid Sci Technol 113(8):1031–1051

    CAS  CrossRef  Google Scholar 

  • Papanikolaou S, Chevalot I, Komaitis M, Aggelis G, Marc I (2001) Kinetic profile of the cellular lipid composition in an oleaginous Yarrowia lipolytica capable of producing a cocoa-butter substitute from industrial fats. Antonie Van Leeuwenhoek 80(3–4):215–224

    CAS  PubMed  CrossRef  Google Scholar 

  • Papanikolaou S, Muniglia L, Chevalot I, Aggelis G, Marc I (2002) Yarrowia lipolytica as a potential producer of citric acid from raw glycerol. J Appl Microbiol 92(4):737–744

    CAS  PubMed  CrossRef  Google Scholar 

  • Papanikolaou S, Sarantou S, Komaitis M, Aggelis G (2004) Repression of reserve lipid turnover in Cunninghamella echinulata and Mortierella isabellina cultivated in multiple-limited media. J Appl Microbiol 97(4):867–875

    CAS  PubMed  CrossRef  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(2):134–142

    CAS  PubMed  CrossRef  Google Scholar 

  • Papanikolaou S, Fakas S, Fick M, Chevalot I, Galiotou-Panayotou M, Komaitis M, Marc I, Aggelis G (2008a) Biotechnological valorisation of raw glycerol discharged after bio-diesel (fatty acid methyl esters) manufacturing process: production of 1,3-propanediol, citric acid and single cell oil. Biomass Bioenergy 32(1):60–71

    CAS  CrossRef  Google Scholar 

  • Papanikolaou S, Galiotou-Panayotou M, Fakas S, Komaitis M, Aggelis G (2008b) Citric acid production by Yarrowia lipolytica cultivated on olive-mill waste water-based media. Bioresour Technol 99(7):2419–2428

    CAS  PubMed  CrossRef  Google Scholar 

  • Papanikolaou S, Chatzifragkou A, Fakas S, Galiotou-Panayotou M, Komaitis M, Nicaud J-M, Aggelis G (2009) Biosynthesis of lipids and organic acids by Yarrowia lipolytica strains cultivated on glucose. Eur J Lipid Sci Technol 111(12):1221–1232

    CAS  CrossRef  Google Scholar 

  • Papanikolaou S, Beopoulos A, Koletti A, Thevenieau F, Koutinas AA, Nicaud JM, Aggelis G (2013) Importance of the methyl-citrate cycle on glycerol metabolism in the yeast Yarrowia lipolytica. J Biotechnol 168(4):303–314

    CAS  PubMed  CrossRef  Google Scholar 

  • Papanikolaou S, Kampisopoulou E, Blanchard F, Rondags E, Gardeli C, Koutinas AA, Chevalot I, Aggelis G (2017) Production of secondary metabolites through glycerol fermentation under carbon-excess conditions by the yeasts Yarrowia lipolytica and Rhodosporidium toruloides. Eur J Lipid Sci Technol 119(9):1600507

    CrossRef  CAS  Google Scholar 

  • Rakicka M, Lazar Z, Rywinska A, Rymowicz W (2016) Efficient utilization of inulin and glycerol as fermentation substrates in erythritol and citric acid production using Yarrowia lipolytica expressing inulinase. Chem Pap 70(11):1452–1459

    CAS  CrossRef  Google Scholar 

  • Rane KD, Sims KA (1993) Production of citric acid by Candida lipolytica Y1095 - effect of glucose-concentration on yield and productivity. Enzym Microb Technol 15(8):646–651

    CAS  CrossRef  Google Scholar 

  • Rane KD, Sims KA (1996) Citric acid production by Yarrowia lipolytica: effect of nitrogen and biomass concentration on yield and productivity. Biotechnol Lett 18(10):1139–1144

    CAS  CrossRef  Google Scholar 

  • Ratledge C (1987) Lipid biotechnology: a wonderland for the microbial physiologist. J Am Oil Chem Soc 64(12):1647–1656

    CAS  CrossRef  Google Scholar 

  • Ratledge, C. 1988. Biochemistry, stoichiometry, substrates and economics in: Single Cell Oil, (Ed.) R.S. Moreton, Longman Scientific & Technical, Longman House Burnt Mill, Harlow and Essex, pp. 33–70

    Google Scholar 

  • Ratledge C, Wynn JP (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51

    CAS  PubMed  CrossRef  Google Scholar 

  • Rodrigues G, Pais C (2000) The influence of acetic and other weak carboxylic acids on growth and cellular death of the yeast Yarrowia lipolytica. Food Technol Biotechnol 38(1):27–32

    CAS  Google Scholar 

  • Roukas T, Kotzekidou P (1997) Pretreatment of date syrup to increase citric acid production. Enzym Microb Technol 21(4):273–276

    CAS  CrossRef  Google Scholar 

  • Rymowicz W, Kautola H, Wojtatowicz M, Linko Y-Y, Linko P (1993) Studies on citric acid production with immobilized Yarrowia lipolytica in repeated batch and continuous air lift bioreactors. Appl Microbiol Biotechnol 39(1):1–4

    CAS  CrossRef  Google Scholar 

  • Rymowicz W, Rywinska A, Zarowska B, Juszczyk P (2006) Citric acid production from raw glycerol by acetate mutants of Yarrowia lipolytica. Chemical Papers-Chemicke Zvesti 60(5):391–394

    CAS  Google Scholar 

  • Rymowicz W, Rywinska A, Gladkowski W (2008) Simultaneous production of citric acid and erythritol from crude glycerol by Yarrowia lipolytica Wratislavia K1. Chem Pap 62(3):239–246

    CAS  CrossRef  Google Scholar 

  • Rymowicz W, Rywinska A, Marcinkiewicz M (2009) High yield production of erythritol from raw glycerol in fed-batch cultures of Yarrowia lipolytica. Biotechnol Lett 31(3):377–380

    CAS  PubMed  CrossRef  Google Scholar 

  • Rymowicz W, Fatykhova AR, Kamzolova SV, Rywinska A, Morgunov IG (2010) Citric acid production from glycerol-containing waste of biodiesel industry by Yarrowia lipolytica in batch, repeated batch, and cell recycle regimes. Appl Microbiol Biotechnol 87(3):971–979

    CAS  PubMed  CrossRef  Google Scholar 

  • Rywinska A, Rymowicz W (2010) High yield production of citric acid by Yarrowia lipolytica on glycerol in repeated batch bioreactors. J Ind Microbiol Biotechnol 37(5):431–435

    CAS  PubMed  CrossRef  Google Scholar 

  • Rywinska A, Rymowicz W, Zarowska B, Wojtatowicz M (2009) Biosynthesis of citric acid from glycerol by acetate mutants of Yarrowia lipolytica in fed batch fermentation. Food Technol Biotechnol 47(1):1–6

    CAS  Google Scholar 

  • Rywinska, A., Rymowicz, W., Marcinkiewicz, M. 2010a. Valorization of raw glycerol for citric acid production by Yarrowia lipolytica yeast. Electron J Biotechnol, 13(4):9–10

    Google Scholar 

  • Rywinska A, Rymowicz W, Zarowska B, Skrzypinski A (2010b) Comparison of citric acid production from glycerol and glucose by different strains of Yarrowia lipolytica. World J Microbiol Biotechnol 26(7):1217–1224

    CAS  PubMed  CrossRef  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(1–2):54–57

    CAS  PubMed  CrossRef  Google Scholar 

  • Rywinska A, Musial I, Rymowicz W, Zarowska B, Boruczkowski T (2012) Effect of agitation and aeration on the citric acid production by Yarrowia lipolytica grown on glycerol. Prep Biochem Biotechnol 42(3):279–291

    CAS  PubMed  CrossRef  Google Scholar 

  • Rywinska A, Juszczyk P, Wojtatowicz M, Robak M, Lazar Z, Tomaszewska L, Rymowicz W (2013) Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass Bioenergy 48:148–166

    CAS  CrossRef  Google Scholar 

  • Rzechonek DA, Dobrowolski A, Rymowicz W, Mironczuk AM (2019) Aseptic production of citric and isocitric acid from crude glycerol by genetically modified Yarrowia lipolytica. Bioresour Technol 271:340–344

    CAS  PubMed  CrossRef  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 waste water based media. J Chem Technol Biotechnol 86(11):1439–1448

    CAS  CrossRef  Google Scholar 

  • Sarris D, Stoforos NG, Mallouchos A, Kookos IK, Koutinas AA, Aggelis G, Papanikolaou S (2017) Production of added value metabolites by Yarrowia lipolytica growing in olive mill wastewater-based media under aseptic and non-aseptic conditions. Eng Life Sci 17(6):695–709

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Show PL, Oladele KO, Siew QY, Zakry FAA, Lan JCW, Ling TC (2015) Overview of citric acid production from Aspergillus niger. Front Life Sci 8(3):271–283

    CAS  CrossRef  Google Scholar 

  • Soccol CR, Vandenberghe LPS, Rodrigues C, Pandey A (2006) New perspectives for citric acid production and application. Food Technol Biotechnol 44(2):141–149

    CAS  Google Scholar 

  • Sun XH, Lu HX, Wang JY (2017) Recovery of citric acid from fermented liquid by bipolar membrane electrodialysis. J Clean Prod 143:250–256

    CAS  CrossRef  Google Scholar 

  • Tan MJ, Chen X, Wang YK, Liu GL, Chi ZM (2016) Enhanced citric acid production by a yeast Yarrowia lipolytica over expressing a pyruvate carboxylase gene. Bioprocess Biosyst Eng 39(8):1289–1296

    CAS  PubMed  CrossRef  Google Scholar 

  • Taskin M, Saghafian A, Aydogan MN, Arslan NP (2015) Microbial lipid production by cold adapted oleaginous yeast Yarrowia lipolytica B9 in non-sterile whey medium. Biofuels Bioprodu Biorefining-Biofpr 9(5):595–605

    CAS  CrossRef  Google Scholar 

  • Timoumi A, Guillouet SE, Molina-Jouve C, Fillaudeau L, Gorret N (2018) Impacts of environmental conditions on product formation and morphology of Yarrowia lipolytica. Appl Microbiol Biotechnol 102(9):3831–3848

    CAS  PubMed  CrossRef  Google Scholar 

  • Tomaszewska L, Rakicka M, Rymowicz W, Rywinska A (2014) A comparative study on glycerol metabolism to erythritol and citric acid in Yarrowia lipolytica yeast cells. FEMS Yeast Res 14(6):966–976

    CAS  PubMed  CrossRef  Google Scholar 

  • Tsigie YA, Wang CY, Truong CT, Ju YH (2011) Lipid production from Yarrowia lipolytica Po1g grown in sugarcane bagasse hydrolysate. Bioresour Technol 102(19):9216–9222

    CAS  PubMed  CrossRef  Google Scholar 

  • Tsigie YA, Wang C-Y, Kasim NS, Diem Q-D, Huynh L-H, Ho Q-P, Truong C-T, Ju Y-H (2012) Oil production from Yarrowia lipolytica Po1g using rice bran hydrolysate. J Biomed Biotechnol 2012:10

    CrossRef  CAS  Google Scholar 

  • Tzirita M, Papanikolaou S, Chatzifragkou A, Quilty B (2018) Waste fat biodegradation and biomodification by Yarrowia lipolytica and a bacterial consortium composed of Bacillus spp. and Pseudomonas putida. Eng Life Sci 18(12):932–942

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Urak S, Yeniay O, Karasu-Yalcin S (2015) Optimization of citric acid production from a carrot juice based medium by Yarrowia lipolytica using response surface methodology. Ann Microbiol 65(2):639–649

    CAS  CrossRef  Google Scholar 

  • Vandenberghe LPS, Soccol CR, Pandey A, Lebeault JM (1999) Microbial production of citric acid. Braz Arch Biol Technol 42(3):263–276

    CAS  CrossRef  Google Scholar 

  • Venter T, Kock JLF, Botes PJ, Smit MS, Hugo A, Joseph M (2004) Acetate enhances citric acid production by Yarrowia lipolytica when grown on sunflower oil. Syst Appl Microbiol 27(2):135–138

    CAS  PubMed  CrossRef  Google Scholar 

  • Wang LF, Wang ZP, Liu XY, Chi ZM (2013) Citric acid production from extract of Jerusalem artichoke tubers by the genetically engineered yeast Yarrowia lipolytica strain 30 and purification of citric acid. Bioprocess Biosyst Eng 36(11):1759–1766

    CAS  PubMed  CrossRef  Google Scholar 

  • Wojtatowicz M, Rymowicz W, Kautola H (1991) Comparison of different strains of the yeast Yarrowia lipolytica for citric acid production from glucose hydrol. Appl Biochem Biotechnol 31(2):165–174

    CAS  PubMed  CrossRef  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 3:58

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Yalcin SK (2012) Enhancing citric acid production of Yarrowia lipolytica by mutagenesis and using natural media containing carrot juice and celery byproducts. Food Sci Biotechnol 21(3):867–874

    CAS  CrossRef  Google Scholar 

  • Yalcin SK, Bozdemir MT, Ozbas ZY (2009) A comparative study on citric acid production kinetics of two Yarrowia lipolytica strains in two different media. Indian J Biotechnol 8(4):408–417

    CAS  Google Scholar 

  • Yalcin SK, Bozdemir M, Ozbas Z (2010a) Citric acid production by yeasts: fermentation conditions, process optimization and strain improvement. Curr Res Technol Educ Top Appl Microbiol Microb Bitechnol 27:1374–1382

    Google Scholar 

  • Yalcin SK, Bozdemir MT, Ozbas ZY (2010b) Effects of different fermentation conditions on growth and citric acid production kinetics of two Yarrowia lipolytica strains. Chem Biochem Eng Q 24(3):347–360

    Google Scholar 

  • Zinjarde S, Apte M, Mohite P, Kumar AR (2014) Yarrowia lipolytica and pollutants: interactions and applications. Biotechnol Adv 32(5):920–933

    CAS  PubMed  CrossRef  Google Scholar 

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Carsanba, E., Papanikolaou, S., Fickers, P., Agirman, B., Erten, H. (2019). Citric Acid Production by Yarrowia lipolytica. In: Sibirny, A. (eds) Non-conventional Yeasts: from Basic Research to Application. Springer, Cham. https://doi.org/10.1007/978-3-030-21110-3_4

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