Skip to main content
Log in

Compositional Shift in Fatty Acid Profiles of Lipids Obtained from Oleaginous Yeasts upon the Addition of Essential Oil from Citrus sinensis L.

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Tailoring lipids from oleaginous yeasts to contain specific types of fatty acid is of considerable interest to food, fuel, and pharmaceutical industries. In this study, the essential oil obtained from Citrus sinesus L. has been used to alter the fatty acid composition of two common oleaginous yeasts, Rhodosporidium toruloides and Cryptococcus curvatus. With increasing levels of essential oil in the medium, the metabolic flux of the fatty acid biosynthesis pathway shifted towards saturated fatty acid production. Essential oil reduced the activities of elongase and ∆9 desaturase. This made the lipid obtained from both these yeasts rich in saturated fatty acids. At certain specific concentrations of the essential oil in the medium, the lipid obtained from R. toruloides and C. curvatus cultures was similar to mahuwa butter and palm oil, respectively. Limonene is the major constituents of orange essential oil. Its effect on one of the oleaginous yeasts, R. toruloides, was also studied separately. Effects similar to orange essential oil were obtained with limonene. Thus, we can conclude that limonene in orange essential oil brings about compositional change of microbial lipid produced in this organism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Uprety, B. K., Chaiwong, W., Ewelike, C., & Rakshit, S. K. (2016). Biodiesel production using heterogeneous catalysts including wood ash and the importance of enhancing byproduct glycerol purity. Energy Conversion and Management, 115, 191–199. doi:10.1016/j.enconman.2016.02.032.

    Article  CAS  Google Scholar 

  2. Uprety, B. K., Dalli, S. S., & Rakshit, S. K. (2017). Bioconversion of crude glycerol to microbial lipid using a robust oleaginous yeast Rhodosporidium toruloides ATCC 10788 capable of growing in the presence of impurities. Energy Conversion and Management, 135, 117–128. doi:10.1016/j.enconman.2016.12.071.

    Article  CAS  Google Scholar 

  3. Christophe, G., Kumar, V., Nouaille, R., Gaudet, G., Fontanille, P., Pandey, A., Soccol, C. R., & Larroche, C. (2012). Recent developments in microbial oils production: a possible alternative to vegetable oils for biodiesel without competition with human food? Brazilian Archives of Biology and Technology, 55(1), 29–46. doi:10.1590/S1516-89132012000100004.

    Article  CAS  Google Scholar 

  4. Moustogianni, A., Bellou, S., Triantaphyllidou, I., & Aggelis, G. (2014). Recent developments in microbial oils production: a possible alternative to vegetable oils for biodiesel without competition with human food? Environmental Biotechnology, 10(1), 1–7. doi:10.14799/ebms237.

    Article  Google Scholar 

  5. Xu, J., Zhao, X., Wang, W., Du, W., & Liu, D. (2012). Microbial conversion of biodiesel byproduct glycerol to triacylglycerols by oleaginous yeast Rhodosporidium toruloides and the individual effect of some impurities on lipid production. Biochemical Engineering Journal, 65, 30–36. doi:10.1016/j.bej.2012.04.003.

    Article  CAS  Google Scholar 

  6. Pyle, D. J., Garcia, R. A., & Wen, Z. (2008). Producing docosahexaenoic acid (DHA)-rich algae from biodiesel-derived crude glycerol: effects of impurities on DHA production and algal biomass composition. Journal of Agricultural and Food Chemistry, 56(11), 3933–3939. doi:10.1021/jf800602s.

    Article  CAS  Google Scholar 

  7. Cao, Y., Liu, W., Xu, X., Zhang, H., Wang, J., & Xian, M. (2014). Production of free monounsaturated fatty acids by metabolically engineered Escherichia coli. Biotechnology for Biofuels, 7(1), 59. doi:10.1186/1754-6834-7-59.

    Article  Google Scholar 

  8. Lipp, M., Simoneau, C., Ulberth, F., Anklam, E., Crews, C., Brereton, P., Greyt, W., Schwack, W., & Wiedmaier, C. (2001). Composition of genuine cocoa butter and cocoa butter equivalents. Journal of Food Composition and Analysis, 14(4), 399–408. doi:10.1006/jfca.2000.0984.

    Article  CAS  Google Scholar 

  9. Papanikolaou, S., Gortzi, O., Margeli, E., Chinou, I., Galiotou-Panayotou, M., & Lalas, S. (2008). Effect of citrus essential oil addition upon growth and cellular lipids of Yarrowia lipolytica yeast. European Journal of Lipid Science and Technology, 110(11), 997–1006. doi:10.1002/ejlt.200800085.

    Article  CAS  Google Scholar 

  10. Sitepu, I. R., Sestric, R., Ignatia, L., Levin, D., German, J. B., Gillies, L. A., Almada, L. A. G., & Boundy-Mills, K. L. (2013). Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresource Technology, 144, 360–369. doi:10.1016/j.biortech.2013.06.047.

    Article  CAS  Google Scholar 

  11. Moustogianni, A., Bellou, S., Triantaphyllidou, I., & Aggelis, G. (2015). Feasibility of raw glycerol conversion into single cell oil by zygomycetes under non-aseptic conditions. Biotechnology and Bioengineering, 112(4), 827–831. doi:10.1002/bit.25482.

    Article  CAS  Google Scholar 

  12. Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods—a review. International Journal of Food Microbiology, 94, 223–253. doi:10.1016/j.ijfoodmicro.2004.03.022.

    Article  CAS  Google Scholar 

  13. Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2008). Biological effects of essential oils—a review. Food and Chemical Toxicology, 46(2), 446–475. doi:10.1016/j.fct.2007.09.106.

    Article  CAS  Google Scholar 

  14. Ghfir, B., Fonvieille, J. L., Koulali, Y., Ecalle, R., & Dargent, R. (1994). Effects of Cymbopogon citratus L. essential oil on the growth, morphogenesis and aflatoxin production of Aspergillus flavus ML2-strain. Mycopathologia, 126(3), 163–167 Retrieved fromhttp://www.ncbi.nlm.nih.gov/pubmed/7935731.

    Article  CAS  Google Scholar 

  15. Helal, G. A., Sarhan, M. M., Abu Shahla, A. N. K., & Abou El-Khair, E. K. (2007). Journal of Basic Microbiology, 47(1), 5–15. doi:10.1002/jobm.200610137.

    Article  CAS  Google Scholar 

  16. Aggelis, G., & Komaitis, M. (1999). Enhancement of single cell oil production by Yarrowia lipolytica growing in the presence of Teucrium polium L. aqueous extract. Biotechnology Letters, 21(9), 747–749. doi:10.1023/A:1005591127592.

    Article  CAS  Google Scholar 

  17. Li, Y. H., Liu, B., Zhao, Z. B., & Bai, F. W. (2006). Optimized culture medium and fermentation conditions for lipid production by Rhodosporidium toruloides. Chinese Journal of Biotechnology, 22(4), 650–656 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16894904.

    Article  CAS  Google Scholar 

  18. Hassan, M., Blanc, P. J., Granger, L.-M., Pareilleux, A., & Goma, G. (1996). Influence of nitrogen and iron limitations on lipid production by Cryptococcus curvatus grown in batch and fed-batch culture. Process Biochemistry, 31(4), 355–361. doi:10.1016/0032-9592(95)00077-1.

    Article  CAS  Google Scholar 

  19. Yu, X., Zheng, Y., Xiong, X., & Chen, S. (2014). Co-utilization of glucose, xylose and cellobiose by the oleaginous yeast Cryptococcus curvatus. Biomass and Bioenergy, 71, 340–349. doi:10.1016/j.biombioe.2014.09.023.

    Article  CAS  Google Scholar 

  20. Wiebe, M. G., Koivuranta, K., Penttilä, M., & Ruohonen, L. (2012). Lipid production in batch and fed-batch cultures of Rhodosporidium toruloides from 5 and 6 carbon carbohydrates. BMC Biotechnology, 12(1), 26. doi:10.1186/1472-6750-12-26.

    Article  CAS  Google Scholar 

  21. Gong, Z., Shen, H., Zhou, W., Wang, Y., Yang, X., & Zhao, Z. K. (2015). Efficient conversion of acetate into lipids by the oleaginous yeast Cryptococcus curvatus. Biotechnology for Biofuels, 8(1), 189. doi:10.1186/s13068-015-0371-3.

    Article  Google Scholar 

  22. Fei, Q., O’Brien, M., Nelson, R., Chen, X., Lowell, A., & Dowe, N. (2016). Enhanced lipid production by Rhodosporidium toruloides using different fed-batch feeding strategies with lignocellulosic hydrolysate as the sole carbon source. Biotechnology for Biofuels, 9(1), 130. doi:10.1186/s13068-016-0542-x.

    Article  Google Scholar 

  23. Liang, Y., Jarosz, K., Wardlow, A. T., Zhang, J., & Cui, Y. (2014). Lipid production by Cryptococcus curvatus on hydrolysates derived from corn fiber and sweet sorghum bagasse following dilute acid pretreatment. Applied Biochemistry and Biotechnology, 173(8), 2086–2098. doi:10.1007/s12010-014-1007-y.

    Article  CAS  Google Scholar 

  24. Ling, J., Nip, S., & Shim, H. (2013). Enhancement of lipid productivity of Rhodosporidium toruloides in distillery wastewater by increasing cell density. Bioresource Technology, 146, 301–309. doi:10.1016/j.biortech.2013.07.023.

    Article  CAS  Google Scholar 

  25. Chi, Z., Zheng, Y., Jiang, A., & Chen, S. (2011). Lipid production by culturing oleaginous yeast and algae with food waste and municipal wastewater in an integrated process. Applied Biochemistry and Biotechnology, 165(2), 442–453. doi:10.1007/s12010-011-9263-6.

    Article  CAS  Google Scholar 

  26. Liang, Y., Cui, Y., Trushenski, J., & Blackburn, J. W. (2010). Converting crude glycerol derived from yellow grease to lipids through yeast fermentation. Bioresource Technology, 101(19), 7581–7586. doi:10.1016/j.biortech.2010.04.061.

    Article  CAS  Google Scholar 

  27. Meesters, P. A. E. P., Huijberts, G. N. M., & Eggink, G. (1996). High-cell-density cultivation of the lipid accumulating yeast Cryptococcus curvatus using glycerol as a carbon source. Applied Microbiology and Biotechnology, 45(5), 575–579. doi:10.1007/s002530050731.

    Article  CAS  Google Scholar 

  28. Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8) Retrieved from http://www.nrcresearchpress.com/doi/pdf/10.1139/o59-099.

  29. Ichihara, K., & Fukubayashi, Y. (2010). Preparation of fatty acid methyl esters for gas-liquid chromatography. Journal of Lipid Research, 51(3), 635–640. doi:10.1194/jlr.D001065.

    Article  CAS  Google Scholar 

  30. Matasyoh, J. C., Wagara, I. N., Nakavuma, J. L., & Kiburai, A. M. (2011). Chemical composition of Cymbopogon citratus essential oil and its effect on mycotoxigenic Aspergillus species. African Journal of Food Science, 5(3), 138–142.

    CAS  Google Scholar 

  31. Helal, G. A., Sarhan, M. M., Abu Shahla, A. N. K., & Abou El-Khair, E. K. (2006). Effects of Cymbopogon citratus L. essential oil on the growth, lipid content and morphogenesis of Aspergillus niger ML2-strain. Journal of Basic Microbiology, 46(6), 456–469. doi:10.1002/jobm.200510106.

    Article  CAS  Google Scholar 

  32. Helal, G. A., Sarhan, M. M., Abu Shahla, A. N. K., & Abou El-Khair, E. K. (2006). Effect of Cymbopogon citratus L. essential oil on growth and morphogenesis of Saccharomyces cerevisiae ML2-strain. Journal of Basic Microbiology, 46(5), 375–386. doi:10.1002/jobm.200510084.

    Article  CAS  Google Scholar 

  33. Verzera, A., Trozzi, A., Dugo, G., Di Bella, G., & Cotroneo, A. (2004). Biological lemon and sweet orange essential oil composition. Flavour and Fragrance Journal, 19(6), 544–548. doi:10.1002/ffj.1348.

    Article  CAS  Google Scholar 

  34. Gao, Z., Ma, Y., Wang, Q., Zhang, M., Wang, J., & Liu, Y. (2016). Effect of crude glycerol impurities on lipid preparation by Rhodosporidium toruloides yeast 32489. Bioresource Technology, 218, 373–379. doi:10.1016/j.biortech.2016.06.088.

    Article  CAS  Google Scholar 

  35. Abghari, A., & Chen, S. (2014). Yarrowia lipolytica as an oleaginous cell factory platform for production of fatty acid-based biofuel and bioproducts. Frontiers in Energy Research, 2, 1–21. doi:10.3389/fenrg.2014.00021.

    Article  Google Scholar 

  36. Thevenieau, F., Beopoulos, A., Desfougeres, T., Sabirova, J., Albertin, K., Zinjarde, S., & Nicaud, J.-M. (2010). Uptake and assimilation of hydrophobic substrates by the oleaginous yeast Yarrowia lipolytica. In Handbook of hydrocarbon and lipid microbiology (pp. 1513–1527). Berlin, Heidelberg: Springer Berlin Heidelberg. doi:10.1007/978-3-540-77587-4_104.

    Chapter  Google Scholar 

  37. Beopoulos, A., & Nicaud, J. M. (2012). Yeast: a new oil producer? Oléagineux, Corps Gras Lipides, 19(1), 22–28. doi:10.1051/ocl.2012.0426.

    Article  Google Scholar 

  38. Beopoulos, A., Nicaud, J. M., & Gaillardin, C. (2011). An overview of lipid metabolism in yeasts and its impact on biotechnological processes. Applied Microbiology and Biotechnology, 90(4), 1193–1206. doi:10.1007/s00253-011-3212-8.

    Article  CAS  Google Scholar 

  39. Moreton, R. S. (1985). Modification of fatty acid composition of lipid accumulating yeasts with cyclopropene fatty acid desaturase inhibitors. Applied Microbiology and Biotechnology, 22, 41–45.

    Article  CAS  Google Scholar 

  40. Shimizu, S., Akimoto, K., Shinmen, Y., Kawashima, H., Sugano, M., & Yamada, H. (1991). Sesamin is a potent and specific inhibitor of Δ5 desaturase in polyunsaturated fatty acid biosynthesis. Lipids, 26(7), 512–516. doi:10.1007/BF02536595.

    Article  CAS  Google Scholar 

  41. 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 Technology and Biotechnology, 38(1), 27–32.

    CAS  Google Scholar 

  42. Hiwale, S. (2015). Mahua (Bassia latifolia Roxb.) In Sustainable horticulture in semiarid dry lands (pp. 255–261). New Delhi: Springer India. doi:10.1007/978-81-322-2244-6_18.

    Google Scholar 

  43. Awasthi, Y. C., Bhatnagar, S. C., Mitra, C. R., & Mitra1, C. R. (n.d.). Chemurgy of sapotaceous plants: Madhuca species of India. Source: Economic Botany, 29(4), 380–389.

  44. Tiwari, S., Saxena, M., & Tiwari, S. K. (2002). Preparation and characterization of penta alkyds based on mahua oil. Journal of Scientific and Industrial Research, 61(2), 110–116.

    CAS  Google Scholar 

  45. Ramadan, M. F., Sharanabasappa, G., Parmjyothi, S., Seshagiri, M., & Moersel, J. T. (2006). Profile and levels of fatty acids and bioactive constituents in mahua butter from fruit-seeds of buttercup tree [Madhuca longifolia (Koenig)]. European Food Research and Technology, 222(5–6), 710–718. doi:10.1007/s00217-005-0155-2.

    Article  CAS  Google Scholar 

  46. Ramadan, M. F., & Moersel, J.T. (2016). Mowrah butter: nature's novel fat. Inform, 17(2).

  47. Panda, H. (2002). Bassia latifolia, Roxb. In H. Panda (Ed.), Medicinal plants cultivation & their uses. Delhi: Asia Pacific Business Press Inc. Retrieved from https://books.google.ca/books?id=xGZNGMTyjOMC&pg=PA218&lpg=PA218&dq=bassia+latifolia+oil+medicinal+use&source=bl&ots=Msco2zHls1&sig=1IvLBEGheGRbRvlHd38DJIiaEpQ&hl=en&sa=X&ved=0ahUKEwja--riqaHPAhVn5oMKHc6CAjoQ6AEILzAD#v=onepage&q=bassia%2520latifolia%2520oil%252.

  48. Hadadare, M., & Salunkhe, V. (2013). Simultaneous estimation of beta sitosterol and palmitic acid from methanolic extract of Caralluma adscedens var fimbriata by UV spectrophotometry. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 4(3), 225–232.

    CAS  Google Scholar 

  49. Rustaiyan, A., Samiee, K., & Vahedi, M. (2012). Lipid content and fatty acid composition in muscle tissue of Perca fluviatilis in the south of the Caspian Sea. Journal of American Science, 8(11), 2000–2003.

    Google Scholar 

  50. Mancini, A., Imperlini, E., Nigro, E., Montagnese, C., Daniele, A., Orru, S., & Buono, P. (2015). Biological and nutritional properties of palm oil and palmitic acid: effects on health. Molecules, 20(9), 17339–17361. doi:10.3390/molecules200917339.

    Article  CAS  Google Scholar 

  51. Gunstone, F. (1996). Fatty acid and lipid chemistry. Fatty acid and lipid chemistry, 2–3.

Download references

Acknowledgements

We would like to express our gratefulness to all the members of Lakehead University Centre for Analytical Services Environmental Laboratory and Lakehead University Instrumentation Laboratory (LUCAS) who helped us carry out certain analysis required as a part of this work. The authors would also like to acknowledge the support of Canada Foundation of Innovation (CFI) and Natural Sciences and Engineering Research Council of Canada (NSERC) for their financial support to undertake the PhD work in this area.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sudip K. Rakshit.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uprety, B.K., Rakshit, S.K. Compositional Shift in Fatty Acid Profiles of Lipids Obtained from Oleaginous Yeasts upon the Addition of Essential Oil from Citrus sinensis L.. Appl Biochem Biotechnol 183, 1158–1172 (2017). https://doi.org/10.1007/s12010-017-2490-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-017-2490-8

Keywords

Navigation