Applied Microbiology and Biotechnology

, Volume 90, Issue 4, pp 1219–1227

Oily yeasts as oleaginous cell factories

  • Jose Manuel Ageitos
  • Juan Andres Vallejo
  • Patricia Veiga-Crespo
  • Tomas G. Villa
Mini-Review

Abstract

Oily yeasts have been described to be able to accumulate lipids up to 20% of their cellular dry weight. These yeasts represent a minor proportion of the total yeast population, and only 5% of them have been reported as able to accumulate more than 25% of lipids. The oily yeast genera include Yarrowia, Candida, Rhodotorula, Rhodosporidium, Cryptococcus, Trichosporon, and Lipomyces. More specifically, examples of oleaginous yeasts include the species: Lipomyces starkeyi, Rhodosporidium toruloides, Rhodotorula glutinis, and Yarrowia lipolytica. Yeast do exhibit advantages for lipid production over other microbial sources, namely, their duplication times are usually lower than 1 h, are much less affected than plants by season or climate conditions, and their cultures are more easily scaled up than those of microalgae. Additionally, some oily yeasts have been reported to accumulate oil up to 80% of their dry weight and can indeed generate different lipids from different carbon sources or from lipids present in the culture media. Thus, they can vary their lipid composition by replacing the fatty acids present in their triglycerides. Due to the diversity of microorganisms and growth conditions, oily yeasts can be useful for the production of triglycerides, surfactants, or polyunsaturated fatty acids.

Keywords

Oleaginous Yeast Cryptococcus Rhodotorula Rodosporidum Candida Lipids Triglycerides 

References

  1. Aggelis G, Sourdis J (1997) Prediction of lipid accumulation-degradation in oleaginous micro-organisms growing on vegetable oils. Antonie Leeuwenhoek 72:159–165CrossRefGoogle Scholar
  2. Angerbauer C, Siebenhofer M, Mittelbach M, Guebitz GM (2008) Conversion of sewage sludge into lipids by Lipomyces starkeyi for biodiesel production. Bioresour Technol 99:3051–3056CrossRefGoogle Scholar
  3. Athenstaedt K, Daum G (2006) The life cycle of neutral lipids: synthesis, storage and degradation. Cell Mol Life Sci 63:1355–1369CrossRefGoogle Scholar
  4. Beopoulos A, Cescut J, Haddouche R, Uribelarrea JL, Molina-Jouve C, Nicaud JM (2009) Yarrowia lipolytica as a model for bio-oil production. Prog Lipid Res 48:375–387CrossRefGoogle Scholar
  5. Botham PA, Ratledge C (1979) A biochemical explanation for lipid accumulation in Candida 107 and other oleaginous micro-organisms. J Gen Microbiol 114:361–375Google Scholar
  6. Boulton CA, Ratledge C (1983) Partial purification and some properties of ATP:citrate lyase from the oleaginous yeast Lipomyces starkeyi. J Gen Microbiol 129:2863–2869Google Scholar
  7. Boulton CA, Ratledge C (1984) Cryptococcus terricolus, an oleaginous yeast re-appraised. Appl Microbiol Biotechnol 20:72–76CrossRefGoogle Scholar
  8. Chistopher T, Scragg AH, Ratledge C (1983) A comparative study of citrate efflux from mitochondria of oleaginous and non oleaginous yeasts. European J Biochem 130:195–204Google Scholar
  9. Daniel HJ, Otto RT, Binder M, Reuss M, Syldatk C (1999) Production of sophorolipids from whey: development of a two-stage process with Cryptococcus curvatus ATCC 20509 and Candida bombicola ATCC 22214 using deproteinized whey concentrates as substrate. Appl Microbiol Biotechnol 51:40–45CrossRefGoogle Scholar
  10. Davies RJ, Holdsworth JE, Reader SL (1990) The effect of low oxygen uptake rate on the fatty acid profile of the oleaginous yeast Apiotrychum curvatum. Appl Microbiol Biotechnol 33:569–573CrossRefGoogle Scholar
  11. Eroshin VK, Krylova NI (1983) Efficiency of lipid synthesis by yeasts. Biotechnol Bioeng 25:1693–1700CrossRefGoogle Scholar
  12. Evans CT, Ratledge C (1983) A comparison of the oleaginous yeast, Candida curvata, grown on different carbon sources in continuous and batch culture. Lipids 18:623–629CrossRefGoogle Scholar
  13. Evans CT, Ratledge C (1984) Phosphofructokinase and the regulation of the flux of carbon from glucose to lipid in the oleaginous yeast Rhodosporidium toruloides. J Gen Microbiol 130:3251–3264Google Scholar
  14. Evans CT, Scragg AH, Ratledge C (1983) A comparative study of citrate efflux from mitochondria of oleaginous and non-oleaginous yeasts. European J Biochem 130:195–204CrossRefGoogle Scholar
  15. Gangar A, Karande AA, Rajasekharan R (2001) Purification and characterization of acyl–acyl carrier protein synthetase from oleaginous yeast and its role in triacylglycerol biosynthesis. Biochem J 360:471–479CrossRefGoogle Scholar
  16. Gill CO, Hall MJ, Ratledge C (1977) Lipid accumulation in an oleaginous yeast (Candida 107) growing on glucose in single-stage continuous culture. Appl Environ Microbiol 33:231–239Google Scholar
  17. Granger LM, Perlot P, Goma G, Pareilleux A (1993) Effect of various nutrient limitations on fatty acid production by Rhodotorula glutinis. Appl Microbiol Biotechnol 38:784–789CrossRefGoogle Scholar
  18. Ham K-S, Rhee J-S (1998) Property characterization and lipid-compositional analysis of lipid granules isolated from an oleaginous yeast Rhodotorula glutinis. J Food Sci Nutr 3:211–215Google Scholar
  19. Hansson L, Dostalek M (1986) Influence of cultivation conditions on lipid production by Cryptococcus albidus. Appl Microbiol Biotechnol 24:12–18Google Scholar
  20. Hassan M, Blanc PJ, Granger L-M, Pareilleux A, Goma G (1993) Lipid production by an unsaturated fatty acid auxotroph of the oleaginous yeast Apiotrichum curvatum grown in single-stated continuous culture. Appl Microbiol Biotechnol 40:483–488CrossRefGoogle Scholar
  21. Hassan M, Blanc PJ, Pareilleux A, Goma G (1994) Selection of fatty acid auxotrophs from the oleaginous yeast Cryptococcus curvatus and production of cocoa butter equivalents in batch culture. Biotechnol Lett 16:819–824CrossRefGoogle Scholar
  22. Heredia L, Ratledge C (1988) Simultaneous utilization of glucose and xylose by Candida curvata D in continuous culture. Biotechnol Lett 10:25–30CrossRefGoogle Scholar
  23. Holdsworth JE, Veenhuis M, Ratledge C (1988) Enzyme activities in oleaginous yeasts accumulating and utilizing exogenous and endogenous lipids. J Gen Microbiol 134:2907–2915Google Scholar
  24. Iassonova DR, Hammond EG, Beattie SE (2008) Oxidative stability of polyunsaturated triacylglycerols encapsulated in oleaginous yeast. J Am Oil Chem Soc 85:711–716CrossRefGoogle Scholar
  25. Jacob Z (1991) Enrichment of wheat bran by Rhodotorula gracilis through solid-state fermentation. Folia Microbiol 36:86–91CrossRefGoogle Scholar
  26. Jacob Z (1992a) Linnear growth and lipid synthesis in the oleaginous yeast Rhodotorula gracilis. Folia Microbiol 37:117–121CrossRefGoogle Scholar
  27. Jacob Z (1992b) Yeast lipids: extraction, quality analysis, and acceptability. Crit Rev Biotechnol 12:463–491CrossRefGoogle Scholar
  28. Jacob Z, Krishnamurlhyb MN (1990) Studies on physicochemical characteristics and fatty acid composition of lipids produced by a strain of Rodotorula gracilis CFR-1. J Am Oil Chem Soc 67:642–645CrossRefGoogle Scholar
  29. Johnson VW, Sigh M, Yadav NK (1992a) Transformation of vegetable oils by an oleaginous yeast: Rodotorula glutinis IIP-30. Biotechnol Lett 14:801–804CrossRefGoogle Scholar
  30. Johnson VW, Singh M, Saini VS, Adhikari DK, SIsta VR, Yadav NK (1992b) Effect of pH on lipid accumulation by an oleaginuous yeast: Rhodotorula glutinis IIP-30. World J Microbiol Biotechnol 8:382–384CrossRefGoogle Scholar
  31. Johnson VW, Sigh M, Saini VS, Adhikari DK, Sista V, Yadav NK (1995) Utilization of molasses for the production of fat by an oleaginous yeast, Rhodotorula glutinis IIP-30. J Ind Microbiol 14:1–4CrossRefGoogle Scholar
  32. Lee I, Hammond EG, Glatz BA (1992) Triacylglycerol assembly from lipid substrates by Apiotrichum curvatum. In: Kyle DJ, Ratledge C (eds) Industrial applications of single cell oils. AOCSPress, Champaign, pp 139–155Google Scholar
  33. Lee I, Hammondl EG, Cornette JL, Glatz BA (1993) Triacylglycerol assembly from binary mixtures of fatty acids by Apiotrychum curvatum. Lipids 28:1055–1061CrossRefGoogle Scholar
  34. Li ZF, Zhang L, Shen XJ, Lai BS, Sun SQ (2001) A comparative study on four method of fungi lipid extraction. Microbiology 28(6):72–75Google Scholar
  35. Li Y-h, Liu B, Sun Y, Z-b Z, F-w B (2005) Screening of oleaginous yeasts for broad-spectrum carbohydrates assimilating capacity. Chin J Biotechnol 25:43–48Google Scholar
  36. Li Y, Zhao Z, Bai F (2007) High-density cultivation of oleaginous yeast Rhodosporidium toruloides Y4 in fed-bach culture. Enzyme Microb Technol 41:312–317CrossRefGoogle Scholar
  37. Li Q, Du W, Liu D (2008) Perspectives of microbial oils for biodiesel production. Appl Microbiol Biotechnol 80:749–756CrossRefGoogle Scholar
  38. Meesters PAEP, Huijberts, Eggink G (1996) High-cell-density cultivation of the lipid accumulating yeast Cryptococcus curvatus using glycerol as a carbon source. Appl Microbiol Biotechnol 45:575–579CrossRefGoogle Scholar
  39. Meesters PAEP, van der Wal H, Weusthuis R, Eggnik G (1996b) Cultivation of the oleaginous yeast Cryptococcus curvatus in a new reactor with improved mixing and mass transfer characteristics (Surer). Biotechnol Tech 10:277–282CrossRefGoogle Scholar
  40. Meng X, Yang J, Xu X, Zhang L, Nie Q, Xian M (2009) Biodiesel production from oleaginous microorganisms. Ren Energi 34:1–5CrossRefGoogle Scholar
  41. Nigam P (1999) Fermentation (industrial)|production of oils and fatty acids. In: Robinson RK (ed) Encyclopaedia of food microbiology. Elsevier, Oxford, pp 718–729CrossRefGoogle Scholar
  42. Pan JG, Rhee JS (1986) Biomass yields and energetic yields of oleaginous yeast in batch culture. Biotechnol Bioeng 28:112–114CrossRefGoogle Scholar
  43. Pan JG, Kwak NY, Rhee JS (1986) High density cell culture of Rhodotorula glutinis using oxygen-enriched air. Biotechnol Lett 8:715–718CrossRefGoogle Scholar
  44. Pan L-X, Yang D-F, Shao L, Li W, Chen G-G, Liang Z-Q (2009) Isolation of the oleaginous yeast from the soil and studies of their lipid-producing capacities. Food Technol Biotechnol 47:215–220Google Scholar
  45. Papanikolaou S, Aggelis G (2002) Lipid production by Yarrowia lipolytica growing on industrial glycerol in a single-stage continuous culture. Bioresour technol 82:43–49CrossRefGoogle Scholar
  46. 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 Leeuwenhoek 80:215–224CrossRefGoogle Scholar
  47. Papanikolaou S, Chevalot I, Komaitis M, Aggelis G, Marc I (2002) Single cell oil production by Yarrowia lipolytica growing on an industrial derivative of animal fat in batch cultures. Appl Microbiol Biotechnol 58:308–312CrossRefGoogle Scholar
  48. Park WS, Murphy P, Glatz BA (1990) Lipid metabolism and cell composition of the oleaginous yeast Apiotrichum curvatum grown at different carbon to nitrogen ratios. Can J Microbiol 36:318–326CrossRefGoogle Scholar
  49. Picataggio SK, Smittle RB (1979) Microbiological production of oil. Eur Pat Appl. EP 5277 A2 19791114Google Scholar
  50. Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 86:807–815CrossRefGoogle Scholar
  51. Rau U, Nguyen LA, Roeper H, Koch H, Lang S (2005) Fed-batch bioreactor production of mannosylerythritol lipids secreted by Pseudozyma aphidis. Appl Microbiol Biotechnol 80:607–613CrossRefGoogle Scholar
  52. Saxena V, Sharma CD, Bhagat SD, Saini VS, Adhikari DK (2008) Lipid and fatty acid biosynthesis by Rhodotorula minuta. J Am Oil Chem Soc 74:501–505Google Scholar
  53. Solaiman DKY, Ashby AD, Nunez A, Foglia TA (2004) Production of sophorolipids by Candida bombicola grown on soy molasses as substrate. Biotechnol Lett 26:1241CrossRefGoogle Scholar
  54. Turcotte G, Kosaric N (1989) Lipid biosynthesis in oleaginous yeasts. Adv Biochem Eng Biotech 40:73–92Google Scholar
  55. Vasudevan PT, Briggs M (2008) Biodiesel production—current state of the art and challenges. J Ind Microbiol Biotechnol 35:421–430CrossRefGoogle Scholar
  56. Ykema A, Verbree EC, Kater MM, Smit H (1988) Optimization of lipid production in the oleaginous yeast Apiotrichum curvatum in whey permeate. Appl Microbiol Biotechnol 29:211–218Google Scholar
  57. Ykema A, Kater MM, Smit H (1989) Lipid production in whey permeate by an unsaturated fatty acid mutant of the oleaginous yeast Apiotrichum cruvatum. Biotechnol Lett 11:477–482CrossRefGoogle Scholar
  58. Yoon SH, Park JS, Rhee JS (1984) Production of NADPH for lipogenesis in oleaginous yeast Rhodotorula glutinis. Sanop Misaengmul Hakhoe Chi 12:247–251Google Scholar
  59. Yousuf A, Sannino F, Addorisio V, Pirozzi D (2010) Microbial conversion of olive oil mill wastewaters into lipids suitable for biodiesel production. J Agr Food Chem 58:8630–8635CrossRefGoogle Scholar
  60. Zhao X, Kong X, Hua Y, Feng B, Zhao ZK (2008) Medium optimization for lipid production through co-fermentation of glucose and xylose by the oleaginous yeast Lipomyces starkeyi. Eur J Lipid Sci Technol 110:405–412CrossRefGoogle Scholar
  61. Zhao X, Hu C, Wu S, Shen H, Zhao ZK (2010) Lipid production by Rhodosporidium toruloides Y4 using different substrate feeding strategies. J Ind Micriobiol Biotech. doi:10.1007/s10295-010-0808-4 Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jose Manuel Ageitos
    • 1
  • Juan Andres Vallejo
    • 1
  • Patricia Veiga-Crespo
    • 1
  • Tomas G. Villa
    • 1
  1. 1.Department of Microbiology and Parasitology, Faculty of PharmacyUniversity of Santiago de CompostelaSantiago de CompostelaSpain

Personalised recommendations