link.springer.com

Microbial production of (2 R ,3 S )-isocitric acid: state of the arts and prospects - Applied Microbiology and Biotechnology

  • ️Morgunov, Igor G.
  • ️Tue Nov 12 2019

  • Abe M, Tabuchi T (1968) Occurrence of biologically active isocitric acid in cultures of yeast. Agric Biol Chem 32(3):392–393. https://doi.org/10.1080/00021369.1968.10859065

    Article  CAS  Google Scholar 

  • Abe M, Tabuchi T, Tanaka M (1970) Studies on organic acid fermentation in yeast. III Accumulation ofisocitric acid in cultures of yeast. J Agr Chem Soc Japan 44:493–498

    CAS  Google Scholar 

  • Akiyama S-I, Suzuki T, Sumino Y, Nakao Y, Fukuda H (1973) Induction and citric acid productivity of fluoroacetate-sensitive mutant strains of Candida lipolytica. Agric Biol Chem 37:879–884

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Anastassiadis S, Rehm H-J (2006a) Continuous citric acid secretion by a high specific pH dependent active transport system in yeast Candida oleophila ATCC 20177. Electron J Biotechnol 8(2). https://doi.org/10.4067/S0717-34582005000200004

  • Anastassiadis S, Rehm H-J (2006b) Oxygen and temperature effect on continuous citric acid secretion in Candida oleophila. Electron J Biotechnol 9(4). https://doi.org/10.4067/S0717-34582006000400010

  • 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. https://doi.org/10.1016/j.jbiotec.2016.05.033

    Article  CAS  PubMed  Google Scholar 

  • Aurich A, Specht R, Müller RA, Stottmeister U, Yovkova V, Otto C, Holz M, Barth G, Heretsch P, Thomas FA, Sicker D, Giannis A (2012) Microbiologically produced carboxylic acids used as building blocks in organic synthesis. In: Wang X, Chen J, Quinn P (eds) Reprogramming Microbial Metabolic Pathways, Subcellular Biochemistry, vol 64. Springer, Dordrecht, pp 391–423

    Google Scholar 

  • Aurich A, Hofmann J, Oltrogge R, Wecks M, Glaser R, Blömer L, Mauersberger S, Roland A, Müller RA, Sicker D, Giannis A (2017) Improved isolation of microbiologically produced (2R,3S)-isocitric acid by adsorption on activated carbon and recovery with methanol. Org Process Res Dev 21:866–870. https://doi.org/10.1021/acs.oprd.7b00090

    Article  CAS  Google Scholar 

  • Barth G, Gaillardin C (1996) Yarrowia lipolytica. In: Wolf K (ed) Non conventional yeasts in biotechnology: a handbook. Springer, Berlin, pp 313–388

    Google Scholar 

  • Barth G, Künkel W (1979) Alcohol dehydrogenase (ADH) in yeasts. II. NAD+-and NADP+-dependent alcohol dehydrogenases in Saccharomycopsis lipolytica. Z Allg Mikrobiol 19(6):381–390

    CAS  PubMed  Google Scholar 

  • Barth G, Beckerich JM, Dominguez A, Kerscher S, Ogrydziak D, Titorenko V, Gaillardin C (2003). Functional genetics of Yarrowia lipolytica. In: Winde JH and Hohmann S (eds) Functional Genetics of Industrial Yeasts. Springer-Verlag, Berlin, Heidelberg, New York. pp. 236-239

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Beppu T, Abe S, Sakaguchi KJ (1957) Accumulation of allo-isocitric acid by a Penicillium strain. J Gen Appl Microbiol 3:225–232

    CAS  Google Scholar 

  • Bullin K, Hennig L, Herold R, Krautscheid H, Richter K, Sicker D (2019) An optimized method for an (2R,3S)-isocitric acid building block. Monatsh Chem 150:247–253. https://doi.org/10.1007/s00706-018-2319-3

    Article  CAS  Google Scholar 

  • Carsanba E, Papanikolaou S, Fickers P, Erten H (2019) Screening various Yarrowia lipolytica strains for citric acid production. Yeast 36(5):319–327. https://doi.org/10.1002/yea.3389

    Article  CAS  PubMed  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). https://doi.org/10.1093/femsyr/fox084

  • Da Silva LV, Tavares CB, Amaral PFF, Coehlo MAZ (2012) Production of citric acid by Yarrowia lipolytica in different crude oil concentrations and in different nitrogen sources. Chem Eng Trans 27:199–204

    Google Scholar 

  • Daskalaki A, Perdikouli N, Aggelis D, Aggelis G (2019) Laboratory evolution strategies for improving lipid accumulation in Yarrowia lipolytica. Appl Microbiol Biotechnol Sep 11 103:8585–8596. https://doi.org/10.1007/s00253-019-10088-7

    Article  CAS  PubMed  Google Scholar 

  • Ermakova IT, Shishkanova NV, Melnikova OF, Finogenova TV (1986) Properties of Candida lipolytica mutants with the modified glyoxylate cycle and their ability to produce citric and isocitric acid. I. Physiological, biochemical and cytological characteristics of mutants grown on glucose or hexadecane. Appl Microbiol Biotechnol 23:372–377

    CAS  Google Scholar 

  • Fickers P, Benetti P-H, Waché Y, Marty A, Mauersberger S, Smit MS, Nicaud J-M (2005) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5 (6-7):527–543.

    CAS  PubMed  Google Scholar 

  • Fickers P, Marty A, Nicaud JM (2011) The lipases from Yarrowia lipolytica: genetics, production, regulation, biochemical characterization and biotechnological applications. Biotechnol Adv 29(6):632–644. https://doi.org/10.1016/j.biotechadv.2011.04.005

    Article  CAS  PubMed  Google Scholar 

  • Finogenova TV (1982) Biosynthesis of organic acids by yeast organisms and its regulation. Dissertation, USSR Academy of Sciences, Institute of Biochemistry and Physiology of Microorganisms (in Russian)

    Google Scholar 

  • Finogenova TV, Shishkanova NV, Ermakova IT, Kataeva IA (1986) Properties of Candida lipolytica mutants with the modified glyoxylate cycle and their ability to produce citric and isocitric acid. II. Synthesis of citric and isocitric acid by mutants and peculiarities of their enzyme systems. Appl Microbiol Biotechnol 23:378–383

    CAS  Google Scholar 

  • Finogenova TV, Shishkanova NV, Illarionova VI. Lozinov AB, Karklin R, Peltzmane I, Yezhov VA (1989) Strain Candida lipolytica HMM-149 as producer of isocitric acid. Patent USSR915466A1

  • Finogenova TV, Shishkanova NV, Fausek EA, Eremina SS (1991) Biosynthesis of isocitric acid from ethanol by yeasts. Appl Microbiol Biotechnol 36(2):231–235. https://doi.org/10.1007/BF00164426

    Article  CAS  Google Scholar 

  • Finogenova TV, Morgunov IG, Kamzolova SV, Chernyavskaya OG (2005) Organic acid production by the yeast Yarrowia lipolytica: a review of prospects. Appl Biochem Microbiol 41:418–425. https://doi.org/10.1007/s10438-005-0076-7

    Article  CAS  Google Scholar 

  • Flores CL, Gancedo C (2005) Yarrowia lipolytica mutants devoid of pyruvate carboxylase activity show an unusual growth phenotype. Eukaryot Cell 4(2):356–364

    CAS  PubMed  PubMed Central  Google Scholar 

  • Förster A, Jacobs K, Juretzek T, Mauersberger S, Barth B (2007) Overexpression of the ICL1 gene changes the product ratio of citric acid production by Yarrowia lipolytica. Appl Microbiol Biotechnol 77:861–869. https://doi.org/10.1007/s00253-007-1205-4

    Article  CAS  PubMed  Google Scholar 

  • Fukuda R (2013) Metabolism of hydrophobic carbon sources and regulation of it in n-alkane-assimilating yeast Yarrowia lipolytica. Biosci Biotechnol Biochem 77(6):1149–1154

    CAS  PubMed  Google Scholar 

  • Fukuda R, Ohta A (2017) Enzymes for aerobic degradation of alkanes in yeasts. In: Rojo F (ed) Aerobic Utilization of Hydrocarbons. Handbook of Hydrocarbon and Lipid Microbiology. Springer International Publishing AG, Oils and Lipids, pp 1–14

    Google Scholar 

  • Gatter M, Förster A, Bär K, Winter M, Otto C, Petzsch P, Ježková M, Bahr K, Pfeiffer M, Matthäus F, Barth G (2014) A newly identified fatty alcohol oxidase gene is mainly responsible for the oxidation of long-chain ω-hydroxy fatty acids in Yarrowia lipolytica. FEMS Yeast Res 14(6):858–872. https://doi.org/10.1111/1567-1364.12176

    Article  CAS  PubMed  Google Scholar 

  • Gatter M, Ottlik S, Kövesi Z, Bauer B, Matthäus F, Barth G (2016) Three alcohol dehydrogenase genes and one acetyl-CoA synthetase gene are responsible for ethanol utilization in Yarrowia lipolytica. Fungal Genet Biol 95:30–38. https://doi.org/10.1016/j.fgb.2016.07.012

    Article  CAS  PubMed  Google Scholar 

  • Good DW, Droniuk R, Lawford GR, Fein JE (1985) Isolation and characterization of a Saccharomycopsis lipolytica mutant showing increased production of citric acid from canola oil. Can J Microbiol 31:436–440. https://doi.org/10.1139/m85-081

    Article  CAS  Google Scholar 

  • Heretsch P, Thomas F, Aurich A, Krautscheid H, Sicker D, Giannis A (2008) Syntheses with a chiral building block from the citric acid cycle: (2R,3S)-isocitric acid by fermentation of sunflower oil. Angew Chem Int Ed Eng 47:1958–1960. https://doi.org/10.1002/anie.200705000

    Article  CAS  Google Scholar 

  • Hirakawa K, Kobayashi S, Inoue T, Endoh-Yamagami S, Fukuda R, Ohta A (2009) Yas3p, an Opi1 family transcription factor, regulates cytochrome P450 expression in response to n-alcanes in Yarrowia lipolytica. J Biol Chem 284:7126–7137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holdsworth JE, Veenhuis H, Ratledge C (1988) Enzyme activities in oleaginous yeasts accumulating and utilizing exogenous or endogenous lipids. J Gen Microbiol 134:2907–2915

    CAS  PubMed  Google Scholar 

  • Holz M, Förster A, Mauersberger S, Barth G (2009) Aconitase overexpression changes the product ratio of citric acid production by Yarrowia lipolytica. Appl Microbiol Biotechnol 81:1087–1096. https://doi.org/10.1007/s00253-008-1725-6

    Article  CAS  PubMed  Google Scholar 

  • Hoshiko S, Kunimoto Y, Arima K, Beppu T (1982) Mechanism of L-alloisocitric acid fermentation: isocitrate epimerase activity in the cell free extract of Penicillum purpurogenum. Agric Biol Chem 46:143–151

    CAS  Google Scholar 

  • Il’chenko AP, Chernyavskaya OG, Shishkanova NV, Finogenova TV (2003) Induction of cytochrome P-450 and ethanol oxidation in Yarrowia lipolytica. Mikrobiologiia 72(2):168–173

    PubMed  Google Scholar 

  • Il’chenko AP, Chernyavskaya OG, Finogenova TV (2005) Ethanol metabolism in the yeasts Yarrowia and Torulopsis: a review. Appl Biochem Microbiol 41:426–432. https://doi.org/10.1007/s10438-005-0077-6

    Article  CAS  Google Scholar 

  • Iwama R, Kobayashi S, Ishimaru C, Ohta A, Horiuchi H, Fukuda R (2016) Functional roles and substrate specificities of twelve cytochromes P450 belonging to CYP52 family in n-alkane assimilating yeast Yarrowia lipolytica. Fungal Genet Biol 91:43–54. https://doi.org/10.1016/j.fgb.2016.03.007

    Article  CAS  PubMed  Google Scholar 

  • Kamzolova SV, Lunina JN, Morgunov IG (2011) Biochemistry of citric acid production from rapeseed oil by Yarrowia lipolytica Yeast. J Am Oil Chem Soc 88:1965–1976. https://doi.org/10.1007/s11746-011-1954-1

    Article  CAS  Google Scholar 

  • Kamzolova SV, Dedyukhina EG, Samoilenko VA, Lunina JN, Puntus IF, Allayarov RK, Chiglintseva MN, Mironov AA, Morgunov IG (2013) Isocitric acid production from rapeseed oil by Yarrowia lipolytica yeast. Appl Microbiol Biotechnol 97:9133–9144. https://doi.org/10.1007/s00253-013-5182-5

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Kamzolova SV, Allayarov RK, Lunina JN, Morgunov IG (2016) The effect of oxalic and itaconic acids on threo-Ds-isocitric acid production from rapeseed oil by Yarrowia lipolytica. Bioresour Technol 206:128–133. https://doi.org/10.1016/j.biortech.2016.01.092

    Article  CAS  PubMed  Google Scholar 

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

  • Kamzolova SV, Shamin RV, Stepanova NN, Morgunov GI, Lunina JN, Allayarov RK, Samoilenko VA, Morgunov IG (2018) Fermentation conditions and media optimization for isocitric acid production from ethanol by Yarrowia lipolytica. Biomed Res Int 2018:2543210. https://doi.org/10.1155/2018/2543210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karklin R, Peltzmane I, Raminya L, Korde G (1991) Overproduction of isocitric acid by wild strain of Candida lipolytica. In: Metabolism of n-Alkanes and Oversynthesis of Products by Microorganisms, Pushchino, Russia, pp. 143–146(in Russian).

  • Karklinsh RJ, Liepinsh GK (1993) Features of the assimilation of n-alkanes. In: Microbial biosynthesis of citric acid. Zinatne, Riga, pp 73–82 (in Russian)

    Google Scholar 

  • Kulkarni MG, Shaikh YB, Borhade AS, Dhondge AP, Chavhan SW, Desai MP, Birhade DR, Dhatrak NR, Gannimani R (2010) The efficient synthesis of (3R,3aS,6aR)-hexahydrofuro[2,3-b]furan-3-ol and its isomers. Tetrahedron Asymmetry 21:2394–2398. https://doi.org/10.1016/j.tetasy.2010.08.005

    Article  CAS  Google Scholar 

  • Laptev IA, Filimonova NA, Allayarov RK, Kamzolova SV, Samoilenko VA, Sineoky SP, Morgunov IG (2016) New recombinant strains of the yeast Yarrowia lipolytica with overexpression of the aconitate hydratase gene for the obtainment of isocitric acid from rapeseed oil. Appl Biochem Microbiol 52:699–704. https://doi.org/10.1134/S000368381607005X

    Article  CAS  Google Scholar 

  • Liu X, Lv J, Xu J, Zhang T, Deng Y, He J (2015a) Citric acid production in Yarrowia lipolytica SWJ-1b yeast when grown on waste cooking oil. Appl Biochem Biotechnol 175(5):2347–2356. https://doi.org/10.1007/s12010-014-1430-0

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Lv J, Zhang T, Deng Y (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. https://doi.org/10.1080/10826068.2014.979203

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Pan A, Spofford C, Zhou N, Alper HS (2015c) An evolutionary metabolic engineering approach for enhancing lipogenesis in Yarrowia lipolytica. MetabEng29:36–45.

  • 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. https://doi.org/10.1016/j.biortech.2009.11.024

    Article  CAS  PubMed  Google Scholar 

  • Marchal R, Metche M, Vandecasteele JP (1980) Intracellular concentrations of citric and isocitric acids in cultures of the citric acid-excreting yeast Saccharomycopsis lipolytica grown on alkanes. J Gen Microbiol 116:535–538

    CAS  Google Scholar 

  • Mauersberger S, Kruse K, Barth G (2003) Chapter 63, Induction of citric acid/isocitric acid and α-ketoglutaric acid production in the yeast Yarrowia lipolytica. In: Wolf K, Breunig K, Barth G (eds) Non-conventional yeasts in genetics, biochemistry and biotechnology. Practical protocols. Springer, Berlin Heidelberg New York, pp 393–400

  • Mirończuk AM, Rzechonek DA, Biegalska A, Rakicka M, Dobrowolski A (2016) A novel strain of Yarrowia lipolytica as a platform for value-added product synthesis from glycerol. Biotechnol Biofuels 9(1):180. https://doi.org/10.1186/s13068-016-0593-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore GL, Stringham RW, Teager DS, Yue TY (2017) Practical synthesis of the bicyclic darunavir side chain: (3R,3aS,6aR)-hexahydrofuro[2,3-b]furan-3-ol from monopotassium isocitrate. Org Process Res Dev 21(1):98–106. https://doi.org/10.1021/acs.oprd.6b00377

    Article  CAS  PubMed  Google Scholar 

  • Morgunov IG, Kamzolova SV (2015) Physiologo-biochemical characteristics of citrate-producing yeast Yarrowia lipolytica grown on glycerol-containing waste of biodiesel industry. Appl Microbiol Biotechnol 99(15):6443–6450. https://doi.org/10.1007/s00253-015-6558-5

    Article  CAS  PubMed  Google Scholar 

  • Morgunov IG, Solodovnikova NY, Sharyshev AA, Kamzolova SV, Finogenova TV (2004a) Regulation of NAD(+)-dependent isocitrate dehydrogenase in the citrate producing yeast Yarrowia lipolytica. Biochemistry (Mosc) 69(12):1391–1398

    CAS  Google Scholar 

  • Morgunov IG, Kamzolova SV, Sokolov AP, Finogenova TV (2004b) The isolation, purification, and some properties of NAD-dependent isocitrate dehydrogenase from the organic acid-producing yeast Yarrowia lipolytica. Mikrobiologiia. 73(3):300–306 Russian

    CAS  PubMed  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. https://doi.org/10.1007/s00253-013-5054-z

    Article  CAS  PubMed  Google Scholar 

  • Morgunov IG, Karpukhina OV, Kamzolova SV, Samoilenko VA, Inozemtsev AN (2018) Investigation of the effect of biologically active threo-Ds-isocitric acid on oxidative stress in Paramecium caudatum. Prep Biochem Biotechnol 48(1):1–5. https://doi.org/10.1080/10826068.2017.1381622

    Article  CAS  PubMed  Google Scholar 

  • Morgunov IG, Kamzolova SV, Karpukhina OV, Bokieva SB, Inozemtsev AN (2019) Biosynthesis of isocitric acid in repeated-batch culture and testing of its stress-protective activity. Appl Microbiol Biotechnol 103(8):3549–3558

    CAS  PubMed  Google Scholar 

  • Nakahara T, Kaimaktchiev AC, Oogaki-Chino M, Uchida Y, Tebuchi T (1987) Isocitric acid production from n-alanes by Candida catenulate. Agric Biol Chem 51:2111–2116

    CAS  Google Scholar 

  • Nakanishi T, Yamamoto M, Kimura K, Tanaka K (1972) Fermentative production of citric acid from n-paraffin by yeasts. J Ferment Technol 50:855–867

    CAS  Google Scholar 

  • Nicaud JM, Madzak C, Van Den Broek P, Gysler C, Duboc P, Niederberger P, Gaillardin C (2002) Protein expression and secretion in the yeast Yarrowia lipolytica. FEMS Yeast Res 2(3):371–379

    CAS  PubMed  Google Scholar 

  • Oogaki M, Inoue M, Kaimaktchiev AC, Nakahara T, Tabuchi T (1984) Production of isocitric acid from glucose by Candida ravautii. Agric Biol Chem 48:789–795

    CAS  Google Scholar 

  • Otto C, Yovkova V, Barth G (2011) Overproduction and secretion of α-ketoglutaric acid by microorganisms. Appl Microbiol Biotechnol 92:689–695

    CAS  PubMed  Google Scholar 

  • Otto C, Holz M, Barth G (2013) Production of organic acids by Yarrowia lipolytica. In: Barth G (ed) Yarrowia lipolytica, Microbiology Monographs, vol 25. Springer, Berlin, Heidelberg, pp 137–151

    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  Google Scholar 

  • Papanikolaou S, Galiotou M, Blanchard F, 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 52:134–139

    CAS  PubMed  Google Scholar 

  • Pignède G, Wang HJ, Fudalej F, Seman M, Gaillardin C, Nicaud JM (2000) Autocloning and amplification of LIP2 in Yarrowia lipolytica. Appl Environ Microbiol 66(8):3283–3289. https://doi.org/10.1128/aem.66.8.3283-3289.2000

    Article  PubMed  PubMed Central  Google Scholar 

  • Rzechonek DA, Dobrowolski A, Rymowicz W, Mirończuk AM (2019) Aseptic production of citric and isocitric acid from crude glycerol by genetically modified Yarrowia lipolytica. Bioresour Technol 271:340–344. https://doi.org/10.1016/j.biortech.2018.09.118

    Article  CAS  PubMed  Google Scholar 

  • Sabra W, Bommareddy RR, Maheshwari G, Papanikolaou S, Zeng AP (2017) Substrates and oxygen dependent citric acid production by Yarrowia lipolytica: insights through transcriptome and fluxome analyses. Microb Cell Factories 16(1):78–14. https://doi.org/10.1186/s12934-017-0690-0

    Article  CAS  Google Scholar 

  • Sakaguchi KJ, Beppu T (1959) Study of allo-isocitric acid fermentation. Arch Biochem Biophys 83:131–140

    CAS  PubMed  Google Scholar 

  • Sakaguchi K, Abe S, Beppu T (1960) Method of producing allo-isocitric acid by fermentation. US Patent 2,949,404 16.08.1960

  • Sekova VY, Isakova EP, Deryabina YI (2015) Biotechnological Applications of the Extremophilic Yeast Yarrowia lipolytica (Review). Prikl Biokhim Mikrobiol 51(3):290–304 (in Russian)

    PubMed  Google Scholar 

  • Shabbir Hussain M, Wheeldon I, Blenner MA (2017) A strong hybrid fatty acid inducible transcriptional sensor built from Yarrowia lipolytica upstream activating and regulatory sequences. Biotechnol J 12(10). https://doi.org/10.1002/biot.201700248

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Stern JR (1957) In: Colowik SP, Kaplan NO (eds) Assay of tricarboxylic acids, vol 3. Methods in Enzymology, N.Y., pp 425–431

    Google Scholar 

  • Stottmeister U, Behrens U, Weissbrodt E, Barth G, Franke-Rinker D, Schulze E (1982) Utilization of paraffins and other noncarbohydrate carbon sources for microbial citric acid synthesis. Z Allg Mikrobiol 22(6):399–424 (in German)

    CAS  PubMed  Google Scholar 

  • Stottmeister U, Aurich A, Wilde H, Andersch J, Schmidt S, Sicker D (2005) White biotechnology for Green chemistry: fermentative 2-oxocarboxylic acids as novel building blocks for subsequent chemical syntheses. J Ind Microbiol Biotechnol 32:651–664. https://doi.org/10.1007/s10295-005-0254-x

    Article  CAS  PubMed  Google Scholar 

  • Strijbis K, Distel B (2010) Intracellular acetyl unit transport in fungal carbon metabolism. Eukaryot Cell 9(12):1809–1815

    CAS  PubMed  PubMed Central  Google Scholar 

  • Syal P, Gupta R (2017) Heterologous expression of lipases YLIP4, YLIP5, YLIP7, YLIP13, and YLIP15 from Yarrowia lipolytica MSR80 in Escherichia coli: substrate specificity, kinetic comparison, and enantioselectivity. Biotechnol Appl Biochem 64(6):851–861. https://doi.org/10.1002/bab.1542

    Article  CAS  PubMed  Google Scholar 

  • Tanaka A, Fukui S (1989) Metabolism of n-alkanes. In: The yeast. Academic, London/San Diego/New York/Berkeley/Boston/Sydney/Tokyo/Toronto, pp 261–287

    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. https://doi.org/10.1007/s00253-018-8870-3

    CAS  PubMed  Google Scholar 

  • Tréton B, Le Dall MT, Heslot H (1978) Excretion of citric and isocitric acid by the yeast Saccharomycopsis lipolytica. Eur J Appl Microbiol Biotechnol 6:67–77

    Google Scholar 

  • Vickery (1962) A suggested new nomenclature for the isomers of isocitric acid. J Biol Chem 237:1739–1741

    CAS  PubMed  Google Scholar 

  • Winkler JD, Kao KC (2014) Recent advances in the evolutionary engineering of industrial biocatalysts. Genomics 104:406–411

    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(1):58. https://doi.org/10.1186/2191-0855-3-58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J, Yan Y, Madzak C, Han B (2017) Harnessing biodiesel-producing microbes: from genetic engineering of lipase to metabolic engineering of fatty acid biosynthetic pathway. Crit Rev Biotechnol 37(1):26–36. https://doi.org/10.3109/07388551.2015.1104531

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Kim MJ, Yoon W, Kim EY, Kim H, Lee Y, Min B, Kang KS, Son JH, Park HT, Chung J, Koh H (2017) Isocitrate protects DJ-1 null dopaminergic cells from oxidative stress through NADP+-dependent isocitrate dehydrogenase (IDH). PLoS Genet 13(8):e1006975. https://doi.org/10.1371/journal.pgen.1006975 eCollection 2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Jagtap SS, Deewan A, Rao CV (2019) pH selectively regulates citric acid and lipid production in Yarrowia lipolytica W29 during nitrogen-limited growth on glucose. J Biotechnol 290:10–15

    CAS  PubMed  Google Scholar 

  • Zhou S, Alper HS (2019) Strategies for directed and adapted evolution aspart of microbial strain engineering. J Chem Technol Biotechnol 94:366–376

    CAS  Google Scholar 

  • Zinjarde SS (2014) Food-related applications of Yarrowia lipolytica. Food Chem 152:1–10. https://doi.org/10.1016/j.foodchem.2013.11.117

    Article  CAS  PubMed  Google Scholar