Abstract
Lipid production by Yarrowia lipolytica W29 in fed-batch mode was investigated by using low-cost substitutable defatted silkworm pupae hydrolysate (DSWPH) as a feedstock. Based on the optimized lipid fermentation conditions, three media (i.e. yeast extract, DSWPH, yeast extract-DSWPH as N sources) were investigated in a batch fermentation process. The DSWPH medium displayed the optimal lipid accumulation ability with lipid yield raised by 16.13%, ratio of unsaturated fatty acids/saturated fatty acids (UFAs/SFAs) improved by 95.70%, and ratio of unsaturated fatty acids in total fatty acids (UFAs/TFAs) increased to 87.23%. The mathematical equations based on experimental data provided a good description of temporal variations such as dry cell weight, glucose consumption, and product formation in the fermentation process. The results showed that the Luedeking–Piret type equation successfully described glucose consumption and lipid accumulation in the batch culture process. A fed-batch fermentation process was then designed based on the model prediction. In the lag phase, rapid biomass growth and lipid accumulation were sequentially achieved with the adjustment of temperature, pH, and dissolved oxygen. Finally, the maximum biomass and lipid productivity were 24.01 g/L and 2.76 g/L/d, respectively. Thus, the DSWPH is a nice and substitutable N source for lipid production by Y. lipolytica W29 in the fed-batch mode.
Similar content being viewed by others
References
Zinjarde, S.S.: Food-related applications of Yarrowia lipolytica. Food. Chem. 152, 1–10 (2014)
Yorimitsu, T., Klionsky, D.J.: Autophagy: molecular machinery for self-eating. Cell. Death. Differ. 12, 1542–1552 (2005)
Makri, A., Fakas, S., Aggelis, G.: Metabolic activities of biotechnological interest in Yarrowia lipolytica grown on glycerol in repeated batch cultures. Bioresour. Technol. 101, 2351–2358 (2010)
Fontanille, P., Kumar, V., Christophe, G., Nouaille, R., Larroche, C.: Bioconversion of volatile fatty acids into lipids by the oleaginous yeast Yarrowia lipolytica. Bioresour. Technol. 114, 443–449 (2012)
Lu, Y., Zhai, Y., Liu, M., Wu, Q.: Biodiesel production from algal oil using cassava (Manihot esculenta Crantz) as feedstock. J. Appl. Phycol. 22, 573–578 (2010)
Taskin, M., Ortucu, S., Aydogan, M.N., Arslan, N.P.: Lipid production from sugar beet molasses under non-aseptic culture conditions using the oleaginous yeast Rhodotorula glutinis TR29. Renew. Energy 99, 198–204 (2016)
Yu, X., Zheng, Y., Dorgan, K.M., Chen, S.: Oil production by oleaginous yeasts using the hydrolysate from pretreatment of wheat straw with dilute sulfuric acid. Bioresour. Technol. 102, 6134–6140 (2011)
Sarris, D., Galiotou-Panayotou, M., Koutinas, A.A., Komaitis, M., Papanikolaou, S.: Citric acid, biomass and cellular lipid production by Yarrowia lipolytica strains cultivated on olive mill wastewater-based media. J. Chem. Technol. Biot. 86, 1439–1448 (2011)
Gao, C.F., Zhai, Y., Ding, Y., Wu, Q.Y.: Application of sweet sorghum for biodiesel production by heterotrophic microalga Chlorella protothecoides. Appl. Energy 87, 756–761 (2010)
Sung, M., Seo, Y.H., Han, S., Han, J.: Biodiesel production from yeast Cryptococcus sp using Jerusalem artichoke. Bioresour. Technol. 155, 77–83 (2014)
Ryu, B., Kim, K., Kim, J., Han, J., Yang, J.: Use of organic waste from the brewery industry for high-density cultivation of the docosahexaenoic acid-rich microalga, Aurantiochytrium sp KRS101. Bioresour. Technol. 129, 351–359 (2013)
Maddipati, P., Atiyeh, H.K., Bellmer, D.D., Huhnke, R.L.: Ethanol production from syngas by Clostridium strain P11 using corn steep liquor as a nutrient replacement to yeast extract. Bioresour. Technol. 102, 6494–6501 (2011)
Shi, X.Y., Li, T.Y., Wang, M., Wu, W.W., Li, W.J., Wu, Q.Y., Wu, F.A., Wang, J.: Converting defatted silkworm pupae by Yarrowia lipolytica for enhanced lipid production. Eur. J. Lipid. Sci. Technol. 119, 201600120 (2017)
Pramanik, B.N., Mirza, U.A., Ing, Y.H., Liu, Y., Bartner, P.L., Weber, P.C., Bose, A.K.: Microwave-enhanced enzyme reaction for protein mapping by mass spectrometry: a new approach to protein digestion in minutes. Protein. Sci. 11, 2676–2687 (2002)
Song, X., Zhang, X., Kuang, C., Zhu, L., Zhao, X.: Batch kinetics and modeling of DHA production by S. limacinum OUC88. Food. Bioprod. Process. 88, 26–30 (2010)
Liu, J.Z., Weng, L.P., Zhang, Q.L., Xu, H., Ji, L.N.: A mathematical model for gluconic acid fermentation by Aspergillus niger. Biochem. Eng. J. 14, 137–141 (2003)
Zheng, F., Hu, B.: Thermo-responsive polymer coated fiber-in-tube capillary microextraction and its application to on-line determination of Co, Ni and Cd by inductively coupled plasma mass spectrometry (ICP-MS). Talanta 85, 1166–1173 (2011)
Mondala, A., Hernandez, R., French, T., Green, M., Mcfarland, L., Ingram, L.: Enhanced microbial oil production by activated sludge microorganisms from sugarcane bagasse hydrolyzate. Renew. Energy 78, 114–118 (2014)
Sattur, A.P., Ng, K.: Production of microbial lipids: I. Development of a mathematical model. Biotechnol. Bioeng. 34, 863–867 (1989)
Leesing, R., Karraphan, P.: Kinetic growth of the isolated oleaginous yeast for microbial lipid production. Afr. J. Biotechnol. 10, 13867–13877 (2011)
Feng, J.F., Huang, Y., Zhao, Q., Chen, Q.X.: Clinical significance of preoperative neutrophil lymphocyte ratio versus platelet lymphocyte ratio in patients with small cell carcinoma of the esophagus. Sci. World. J. 4, 504365 (2013)
Xu, K., Xu, P.: Betaine and beet molasses enhance l-lactic acid production by Bacillus coagulans. PLoS ONE 9, e100731 (2014)
Wang, J., Wu, W., Wang, X., Wang, M., Wu, F.: An effective GC method for the determination of the fatty acid composition in silkworm pupae oil using a two-step methylation process. J. Serb. Chem. Soc. 80, 9–20 (2015)
Yu, X., Dong, T., Zheng, Y., Miao, C., Chen, S.: Investigation of cell disruption methods for lipid extraction from oleaginous microorganisms. Eur. J. Lipid. Sci. Technol. 16, 31–32 (2014)
Yang, Z.K., Niu, Y.F., Ma, Y.H., Jiao, X., Zhang, M.H., Yang, W.D., Liu, J.S., Lu, S.H., Guan, Y., Li, H.Y.: Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol. Biofuels 6, 1–14 (2013)
Mlícková, K., Roux, E., Athenstaedt, K., D’Andrea, S., Daum, G., Chardot, T., Nicaud, J.M.: Lipid accumulation, lipid body formation, and acyl coenzyme A oxidases of the yeast Yarrowia lipolytica. Appl. Environ. Microb. 70, 3918–3924 (2004)
Hamid, A.A., Mokhtar, N.F., Taha, E.M., Omar, O., Wan, M.W.Y.: The role of ATP citrate lyase, malic enzyme and fatty acid synthase in the regulation of lipid accumulation in Cunninghamella sp. 2A1. Ann. Microbiol. 61, 463–468 (2011)
Garay, L.A., Boundymills, K.L., German, J.B.: Accumulation of high-value lipids in single-cell microorganisms:a mechanistic approach and future perspectives. J. Agr. Food. Chem. 62, 2709–2727 (2014)
Elbaky, H.H.A., Elbaroty, G.S., Bouaid, A., Martinez, M., Aracil, J.: Enhancement of lipid accumulation in Scenedesmus obliquus by optimizing CO2 and Fe3+ levels for biodiesel production. Bioresour. Technol. 119, 429–432 (2012)
Manikan, V., Kalil, S., Omar, O., Jalil, A.: Aidil: Effects of Mg2+, Fe3+, Mn2+ and Cu2+ ions on lipid accumulation by Cunninghamella bainieri 2A1. Sains. Malays. 43, 443–449 (2014)
Beopoulos, A., Cescut, J., Haddouche, R., Uribelarrea, J., Molina-Jouve, C., Nicaud, J.: Yarrowia lipolytica as a model for bio-oil production. Prog. Lipid. Res. 48, 375–387 (2009)
Mba, O.I., Dumont, M.J., Ngadi, M.: Palm oil: processing, characterization and utilization in the food industry—a review. Food. Biosci. 10, 26–41 (2015)
Ratledge, C., Wynn, J.P.: The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv. Appl. Microbiol. 51, 1–51 (2002)
Beligon, V., Poughon, L., Christophe, G., Lebert, A., Larroche, C., Fontanille, P.: Improvement and modeling of culture parameters to enhance biomass and lipid production by the oleaginous yeast Cryptococcus curvatus grown on acetate. Bioresour. Technol. 192, 582–591 (2015)
Xu, J., Zhao, X., Wang, W., Du, W., Liu, D.: Microbial conversion of biodiesel byproduct glycerol to triacylglycerols by oleaginous yeast Rhodosporidium toruloides and the individual effect of some impurities on lipid production. Biochem. Eng. J. 65, 30–36 (2012)
Ageitos, J.M., Vallejo, J.A., Veiga-Crespo, P., Villa, T.G.: Oily yeasts as oleaginous cell factories. Appl. Microbiol. Biot. 90, 1219–1227 (2011)
Saenge, C., Cheirsilp, B., Bourtoom, T.: Efficient concomitant production of lipids and carotenoids by oleaginous red yeast Rhodotorula glutinis cultured in palm oil mill effluent and application of lipids for biodiesel production. Biotechnol. Bioprocess Eng. 16, 23–33 (2011)
Ferrante, G., Ohno, Y., Kates, M.: Influence of temperature and growth phase on desaturase activity of the mesophilic yeast Candida lipolytica. Can. J. Biochem. Cell. Biol. 61, 171–177 (1983)
Ochoa-Estopier, A., Guillouet, S.E.: 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 (2014)
Papanikolaou, S., Aggelis, G.: Lipids of oleaginous yeasts. Part I: biochemistry of single cell oil production. Eur. J. Lipid. Sci. Tech. 113, 1031–1051 (2011)
Papanikolaou, S., Aggelis, G.: Lipid production by Yarrowia lipolytica growing on industrial glycerol in a single-stage continuous culture. Bioresour. Technol. 82, 43–49 (2002)
Rakicka, M., Lazar, Z., Dulermo, T., Fickers, P., Nicaud, J.M.: Lipid production by the oleaginous yeast Yarrowia lipolytica using industrial by-products under different culture conditions. Biotechnol. Biofuels 8, 104 (2015)
Acknowledgements
This study was financially supported by the Key Research and Development Program (Modern Agriculture) of Jiangsu Province (BE2017322), the Six Talent Peaks Project of Jiangsu Province (2015-NY-018), the Qing Lan Project of Jiangsu Province (2014), the Shen Lan Young scholars program of Jiangsu University of Science and Technology (2015), and the China Agriculture Research System (CARS-18- ZJ0305).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared no conflict of interest.
Electronic Supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xu, XH., Liu, ZX., Shi, XY. et al. Fed-Batch Fermentation of Yarrowia Lipolytica Using Defatted Silkworm Pupae Hydrolysate: A Dynamic Model-Based Approach for High Yield of Lipid Production. Waste Biomass Valor 9, 2399–2411 (2018). https://doi.org/10.1007/s12649-017-0180-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-017-0180-y