Uptake and Assimilation of Hydrophobic Substrates by the Oleaginous Yeast Yarrowia lipolytica

  • France Thevenieau
  • Athanasios Beopoulos
  • Thomas Desfougeres
  • Julia Sabirova
  • Koos Albertin
  • Smita Zinjarde
  • Jean Marc Nicaud
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


The transport of hydrophobic substrates such as fatty acids, triglycerides, and alkanes into a microbial cell has recently begun to receive interest by the scientific community, especially due to the potential biotechnological applications. Here we present an overview on how this process is likely to proceed in the oleaginous yeast Yarrowia lipolytica, an organism which is known to inhabit various lipid containing environments. It is, therefore, well adapted to utilizing these hydrophobic substrates, a process involving firstly their transport into the cells followed by their entry into the subsequent metabolic pathways. Among the strategies employed by Yarrowia in response to exposure to hydrophobic substances are surface-mediated and direct interfacial transport processes, production of biosurfactants, hydrophobisation of the cytoplasmic membrane and the formation of protrusions. Several transport systems have been found to be essential for the growth on hydrophobic compounds, these being either involved in importing the hydrophobic substrate, or in exporting cellular intermediates in order to maintain intracellular concentrations of such compounds at non-toxic levels. Finally, this review also discusses recent advances on the metabolic fate of hydrophobic compounds inside the cell: their terminal oxidation, further degradation or accumulation in the form of intracellular lipid bodies.


  1. Barth G, Gaillardin C (1996) Yarrowia lipolytica. In: Wolf K (ed) Nonconventional yeasts in biotechnology: a handbook. Springer, Heidelberg, pp 313–388CrossRefGoogle Scholar
  2. Barth G, Beckerich JM, Dominguez A, Kerscher S, Ogrydziak D, Titorenko V, Gaillardin C (2003) Functional genetics of Yarrowia lipolytica. In: de Winde JH (ed) Functional genetics of industrial yeasts. Springer, Berlin, pp 227–271CrossRefGoogle Scholar
  3. Cirigliano M, Carman GM (1984) Isolation of a bioemulsifer from Candida lipolytica. Appl Environ Microbiol 48:747–750PubMedPubMedCentralGoogle Scholar
  4. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, De Montigny J, Marck C, Neuveglise C, Talla E, Goffard N, Frangeul L, Aigle M, Anthouard V, Babour A, Barbe V, Barnay S, Blanchin S, Beckerich JM, Beyne E, Bleykasten C, Boisrame A, Boyer J, Cattolico L, Confanioleri F, De Daruvar A, Despons L, Fabre E, Fairhead C, Ferry-Dumazet H, Groppi A, Hantraye F, Hennequin C, Jauniaux N, Joyet P, Kachouri R, Kerrest A, Koszul R, Lemaire M, Lesur I, Ma L, Muller H, Nicaud JM, Nikolski M, Oztas S, Ozier-Kalogeropoulos O, Pellenz S, Potier S, Richard GF, Straub ML, Suleau A, Swennen D, Tekaia F, Wesolowski-Louvel M, Westhof E, Wirth B, Zeniou-Meyer M, Zivanovic I, Bolotin-Fukuhara M, Thierry A, Bouchier C, Caudron B, Scarpelli C, Gaillardin C, Weissenbach J, Wincker P, Souciet JL (2004) Genome evolution in yeasts. Nature 430:35–44CrossRefPubMedGoogle Scholar
  5. Faergeman NJ, DiRusso CC, Elberger A, Knudsen J, Black PN (1997) Disruption of the Saccharomyces cerevisiae homologue to the murine fatty acid transport protein impairs uptake and growth on long-chain fatty acids. J Biol Chem 272:8531–8538CrossRefPubMedGoogle Scholar
  6. Fickers P, Benetti PH, Wache Y, Marty A, Mauersberger S, Smit MS, Nicaud JM (2005a) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:527–543CrossRefPubMedGoogle Scholar
  7. Fickers P, Fudalej F, Le Dall MT, Casaregola S, Gaillardin C, Thonart P, Nicaud JM (2005b) Identification and characterisation of LIP7 and LIP8 genes encoding two extracellular triacylglycerol lipases in the yeast Yarrowia lipolytica. Fungal Genet Biol 42:264–274CrossRefPubMedGoogle Scholar
  8. Guo T, Kit YY, Nicaud JM, Le Dall MT, Sears SK, Vali H, Chan H, Rachubinski RA, Titorenko VI (2003) Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome. J Cell Biol 162:1255–1266CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hadeball W (1991) Production of lipase by Yarrowia lipolytica. Acta Biotechnol 11:159–167CrossRefGoogle Scholar
  10. Hanley K, Nguyen LV, Khan F, Pogue GP, Vojdani F, Panda S, Pinot F, Oriedo VB, Rasochova L, Subramanian M, Miller B, White EL (2003) Development of a plant viral-vector-based gene expression assay for the screening of yeast cytochrome P450 monooxygenases. Assay Drug Dev Technol 1:147–160CrossRefPubMedGoogle Scholar
  11. Iida T, Ohta A, Takagi M (1998) Cloning and characterization of an n-alkane-inducible cytochrome P450 gene essential for n-Decane assimilation by Yarrowia lipolytica. Yeast 14:1387–1397CrossRefPubMedGoogle Scholar
  12. Johnson DR, Knoll LJ, Levin DE, Gordon JI (1994) Saccharomyces cerevisiae contains four fatty acid activation (FAA) genes: an assessment of their role in regulating protein N-myristoylation and cellular lipid metabolism. J Cell Biol 127:751–762CrossRefPubMedGoogle Scholar
  13. Klug MJ, Markovetz AJ (1967) Degradation of hydrocarbons by members of the genus Candida. II. Oxidation of n-alkanes and l-alkenes by Candida lipolytica. J Bacteriol 93:1847–1852PubMedPubMedCentralGoogle Scholar
  14. Knoll LJ, Johnson DR, Gordon JI (1995) Complementation of Saccharomyces cerevisiae strains containing fatty acid activation gene (FAA) deletions with a mammalian acyl-CoA synthetase. J Biol Chem 270:10861–10867CrossRefPubMedGoogle Scholar
  15. Kohlwein S, Paltauf F (1984) Uptake of fatty acids by the yeasts, Saccharomyces uvarum and Saccharomycopsis lipolytica. Biochim Biophys Acta 792:310–317CrossRefPubMedGoogle Scholar
  16. Mauersberger S, Wang HJ, Gaillardin C, Barth G, Nicaud JM (2001) Insertional mutagenesis in the n-alkane-assimilating yeast Yarrowia lipolytica: generation of tagged mutations in genes involved in hydrophobic substrate utilization. J Bacteriol 183:5102–5109CrossRefPubMedPubMedCentralGoogle Scholar
  17. Mlickova K, Roux E, Athenstaedt K, d’Andrea S, Daum G, Chardot T, Nicaud JM (2004) Lipid accumulation, lipid body formation, and acyl coenzyme A oxidases of the yeast Yarrowia lipolytica. Appl Environ Microbiol 70:3918–3924CrossRefPubMedPubMedCentralGoogle Scholar
  18. Nuttley WM, Brade A, Gaillardin C, Eitzen G, Glover J, Aitchison J, Rachubinski R (1993) Rapid identification and characterization of peroxisomal assembly mutants in Yarrowia lipolytica. Yeast 9:507–517CrossRefGoogle Scholar
  19. Osumi M, Fukuzumi F, Yamada N, Nagatani T, Teranishi Y, Tanaka A, Fukui S (1975) Surface structure of some Candida yeast cells grown on n-alkanes. J Ferment Technol 53:244–248Google Scholar
  20. Papanikolaou S, Aggelis G (2003) Modeling lipid accumulation and degradation in Yarrowia lipolytica cultivated on industrial fats. Curr Microbiol 46:398–402CrossRefPubMedGoogle Scholar
  21. Ratledge C (1994) Yeasts, moulds, algae and bacteria as sources of lipids. In: Kamel BS, Kakuda Y (eds) Technological advances in improved and alternative sources of lipids. Blackie Academic and Professional, London, pp 235–291CrossRefGoogle Scholar
  22. Tanaka A, Fukui S (1989) Metabolism of n-alkanes. In: Rose AH, Harrison JS (eds) The yeasts, Metabolism and physiology of yeasts, vol 3, 2nd edn. Academic, London, pp 261–287Google Scholar
  23. Thevenieau F (2006) Metabolic engineering of the yeast Yarrowia lipolytica for the production of long-chain dicarboxylic acids from renewable oil feedstock. Ph.D. thesis, Institut National Agronomique Paris-GrignonGoogle Scholar
  24. Thevenieau F, Le Dall MT, Nthangeni B, Mauersberger S, Marchal R, Nicaud JM (2007) Characterization of Yarrowia lipolytica mutants affected in hydrophobic substrate utilization. Fungal Genet Biol 44:531–542CrossRefPubMedGoogle Scholar
  25. Thevenieau F, Nicaud JM, Gaillardin C (2009) Application of the non-conventional yeast Yarrowia lipolytica. In: Satyanarayana T, Kunze G (eds) Yeast biotechnology: diversity and applications. Springer part III, chapter 26.Google Scholar
  26. Titorenko VI, Nicaud JM, Wang H, Chan H, Rachubinski RA (2002) Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J Cell Biol 156:481–494CrossRefPubMedPubMedCentralGoogle Scholar
  27. Vance-Harrop M, Gusmao N, Campos-Takaki GM (2003) New bioemulsifiers produced by Candida lipolytica using D-glucose and babassu oil as carbon sources. Braz J Microbiol 34:120–123CrossRefGoogle Scholar
  28. Wang H, Le Dall MT, Wache Y, Laroche C, Belin JM, Nicaud JM (1999) Cloning, sequencing, and characterization of five genes coding for acyl-CoA oxidase isozymes in the yeast Yarrowia lipolytica. Cell Biochem Biophys 31:165–174CrossRefPubMedGoogle Scholar
  29. Zinjarde SS, Pant A (2002) Emulsifier from a tropical marine yeast, Yarrowia lipolytica NCIM 3589. J Basic Microbiol 42:67–73CrossRefPubMedGoogle Scholar
  30. Zinjarde SS, Sativel C, Lachke AH, Pant A (1997) Isolation of an emulsifier from Yarrowia lipolytica NCIM 3589 using a modified mini isoelectric focusing unit. Lett Appl Microbiol 24:117–121CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • France Thevenieau
    • 1
    • 5
  • Athanasios Beopoulos
    • 1
  • Thomas Desfougeres
    • 1
  • Julia Sabirova
    • 2
  • Koos Albertin
    • 3
  • Smita Zinjarde
    • 4
  • Jean Marc Nicaud
    • 1
  1. 1.Laboratoire de Microbiologie et Génétique Moléculaire, AgroParisTechCentre de Biotechnologie Agro-IndustrielleThiverval-GrignonFrance
  2. 2.Laboratory of Industrial Microbiology and Biocatalysis, Department of Biochemical and Microbial Technology, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium
  3. 3.Department of Microbial, Biochemical and Food BiotechnologyUniversity of the Free StateBloemfonteinSouth Africa
  4. 4.Institute of Bioinformatics and BiotechnologyUniversity of PunePuneIndia
  5. 5.Oxyrane UK Limited, Greenheys HouseManchester Science ParkManchesterUK

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