Skip to main content
Log in

Erythritol biosynthesis from glycerol by Yarrowia lipolytica yeast: effect of osmotic pressure

  • Original Paper
  • Published:
Chemical Papers Aims and scope Submit manuscript

Abstract

The aim of this study was to examine the impact of osmotic pressure, regulated by an addition of different NaCl concentrations, on the production parameters and activity of the enzymes involved in the biosynthesis of erythritol from glycerol by Yarrowia lipolytica yeast. In the bioreactor batchcultures, strain A-3 was able to produce from 25.3 g dm−3 to 84.7 g dm−3 of erythritol from 150 g dm−3 of glycerol depending on the initial osmotic pressure. At the osmolality of 4.2 mol kg−3 or higher, a long lag-phase was observed. An enhancement of the production parameters was observed in a culture with the osmotic pressure maintained at an equal level by a step-wise addition of NaCl. The two-hour exposure of strain A-3 cells to 75 g dm−3 of NaCl resulted in decreased activity of glycerol kinase and glycerol-3-phosphate dehydrogenase by about 78 % and 25 %, respectively. The activity of transketolase and erythrose reductase remained unchanged after the salt addition. It was demonstrated that assimilation of glycerol was effective at lower osmotic pressures and that transketolase and erythrose reductase played a significant role in the erythritol formation in Y. lipolytica.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Adler, L., Blomberg, A., & Nilsson, A. (1985). Glycerol metabolism and osmoregulation in the salt-tolerant yeast Debaryomyces hansenii. Journal of Bacteriology, 162, 300–306.

    CAS  Google Scholar 

  • Albertyn, J., Hohmann, S., & Prior, B. A. (1994). Characterization of the osmotic-stress response in Saccharomyces cerevisiae: Osmotic stress and glucose repression regulate glycerol-3-phosphate dehydrogenase independently. Current Genetics, 25, 12–18. DOI: 10.1007/bf00712960.

    Article  CAS  Google Scholar 

  • Andreishcheva, E. N., Isakova, E. P., Sidorov, N. N., Abramova, N. B., Ushakova, N. A., Shaposhnikov, G. L, Soares, M. I. M., & Zvyagilskaya, R. A. (1999). Adaptation to salt stress in a salt-tolerant strain of the yeast Yarrowia lipolytica. Biochemistry (Moscow), 64, 1061–1067.

    CAS  Google Scholar 

  • Betts, G. D., Linton, P., & Betteridge, R. J. (1999). Food spoilage yeasts: Effects of pH, NaCl and temperature on growth. Food Control, 10, 27–33. DOI: 10.1016/s0956-7135(98)00151-0.

    Article  Google Scholar 

  • Blomberg, A., & Adler, L. (1992). Physiology of osmotolerance in fungi. Advances in Microbial Physiology, 33, 145–212. DOI: 10.1016/s0065-2911(08)60217-9.

    Article  CAS  Google Scholar 

  • Cho, C. H., Kim, S. Y., Noh, B. S., & Oh, D. K. (1999). Effect of osmotic pressure of salts on erythritol production by Pichia sp. Food Science and Biotechnology, 8, 73–77.

    Google Scholar 

  • Kamzolova, S. V., Finogenova, T. V., & Morgunov, I. G. (2008). Microbiological production of citric and isocitric acids from sunflower oil. Food Technology and Biotechnology, 46, 51–59.

    CAS  Google Scholar 

  • Kayingo, G., Kilian, S. G., & Prior, B. A. (2001). Conservation and release of osmolytes by yeast during hypo-osmotic stress. Archives of Microbiology, 177, 29–35. DOI 10.1007/s00203-001-0358-2.

    Article  CAS  Google Scholar 

  • Kim, S. Y., Lee, K. H., Kim, J. H., & Oh, D. K. (1997). Erythritol production by controlling osmotic pressure in Trigonopsis variabilis. Biotechnology Letters, 19, 727–729. DOI: 10.1023/a:1018371722456.

    Article  CAS  Google Scholar 

  • Kim, S. Y., Oh, D. K., & Jung, S. R. (1999a). U.S. Patent No. 6,001,616. Washington, D.C.: U.S. Patent and Trademark Office.

    Google Scholar 

  • Kim, K. A., Noh, B. S., Kim, S. Y., & Oh, D. K. (1999b). Effect of osmotic pressure of salts on growth of Torula sp. and erythritol production. Korean Journal of Applied Microbiology and Biotechnology, 27, 91–95.

    CAS  Google Scholar 

  • Kim, J. W., Park, T. J., Ryu, D. D. Y., & Kim, J. Y. (2000). High cell density culture of Yarrowia lipolytica using a onestep feeding process. Biotechnology Progress, 16, 657–660. DOI: 10.1021/bp000037n.

    Article  CAS  Google Scholar 

  • Lee, J. K., Ha, S. J., Kim, S. Y., & Oh, D. K. (2000). Increased erythritol production in Torula sp. by Mn2+ and Cu2+. Biotechnology Letters, 22, 983–986. DOI: 10.1023/a:100567 2801826.

    Article  CAS  Google Scholar 

  • Lee, J. K., Ha, S. J., Kim, S. Y., & Oh, D. K. (2001). Increased erythritol production in Torula sp. with inositol and phytic acid. Biotechnology Letters, 23, 497–500. DOI: 10.1023/a:1010386500326.

    Article  CAS  Google Scholar 

  • Lee, J. K., Koo, B. S., & Kim, S. Y. (2002). Fumarate-mediated inhibition of erythrose reductase, a key enzyme for erythritol production by Torula corallina. Applied and Environmental Microbiology, 68, 4534–4538. DOI: 10.1128/aem.68.9.4534-4538.2002.

    Article  CAS  Google Scholar 

  • Lee, J. K., Kim, S. Y., Ryu, Y. W., Seo, J. H., & Kim, J. H. (2003). Purification and characterization of a novel erythrose reductase from Candida magnoliae. Applied and Environmental Microbiology, 69, 3710–3718. DOI: 10.1128/aem.69. 7.3710-3718.2003.

    Article  CAS  Google Scholar 

  • Lin, S. J., Wen, C. Y., Liau, J. C., & Chu, W. S. (2001). Screening and production of erythritol by newly isolated osmophilic yeast-like fungi. Process Biochemistry, 36, 1249–1258. DOI: 10.1016/s0032-9592(01)00169-8.

    Article  CAS  Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193, 265–275.

    CAS  Google Scholar 

  • Lucca, M. E., Spencer, J. F. T., & de Figueroa, L. I. C. (2002). Glycerol and arabitol production by an intergeneric hybrid, PB2, obtained by protoplast fusion between Saccharomyces cerevisiae and Torulaspora delbrueckii. Applied Microbiology and Biotechnology, 59, 472–476. DOI: 10.1007/s00253-002-1025-5.

    Article  CAS  Google Scholar 

  • Makri, A., Fakas, S., & Aggelis, G. (2010). Metabolic activities of biotechnological interest in Yarrowia lipolytica grown on glycerol in repeated batch cultures. Bioresource Technology, 101, 2351–2358. DOI: 10.1016/j.biortech.2009.11.024.

    Article  CAS  Google Scholar 

  • Moon, H. J., Jeya, M., Kim, I. W., & Lee, J. K. (2010). Biotechnological production of erythritol and its applications. Applied Microbiology and Biotechnology, 86, 1017–1025. DOI: 10.1007/s00253-010-2496-4.

    Article  CAS  Google Scholar 

  • Nevoigt, E., & Stahl, U. (1997). Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiology Reviews, 21, 231–241. DOI: 10.1016/s0168-6445(97)00058-2.

    Article  CAS  Google Scholar 

  • Oh, D. K., Cho, C. H., Lee, J. K., & Kim, S. Y. (2001). Increased erythritol production in fed-batch cultures of Torula sp. by controlling glucose concentration. Journal of Industrial Microbiology and Biotechnology, 26, 248–252. DOI: 10.1038/sj.jim.7000122.

    Article  CAS  Google Scholar 

  • Park, J. B., Seo, B. C., Kim, J. R., & Park, Y. K. (1998). Production of erythritol in fed-batch cultures of Trichosporon sp. Journal of Fermentation and Bioengineering, 86, 577–580. DOI: 10.1016/s0922-338x(99)80010-5.

    Article  CAS  Google Scholar 

  • Park, Y. C., Lee, D. Y., Lee, D. H., Kim, H. J., Ryu, Y.W., & Seo, J. H. (2005). Proteomics and physiology of erythritolproducing strains. Journal of Chromatography B, 815, 251–260. DOI: 10.1016/j.jchromb.2004.10.065.

    Article  CAS  Google Scholar 

  • Park, E. H., Lee, H. Y., Ryu, Y. W., Seo, J. H., & Kim, M. D. (2011). Role of osmotic and salt stress in the expression of erythrose reductase in Candida magnoliae. Journal of Microbiology and Biotechnology, 21, 1064–1068. DOI: 10.4014/jmb.1105.05029.

    Article  CAS  Google Scholar 

  • R¨oper, H., & Goossens, J. (1993). Erythritol, a new raw material for food and non-food applications. Starch–Stärke, 45, 400–405. DOI: 10.1002/star.19930451107.

    Article  Google Scholar 

  • Rymowicz, W., Rywi´nska, A., & Marcinkiewicz, M. (2009). High-yield production of erythritol from raw glycerol in fedbatch cultures of Yarrowia lipolytica. Biotechnol Letters, 31, 377–380. DOI: 10.1007/s10529-008-9884-1.

    Article  CAS  Google Scholar 

  • Rywi´nska, A., Juszczyk, P., Wojtatowicz, M., Robak, M., Lazar, Z., Tomaszewska, L., & Rymowicz, W. (2013). Glycerol as a promising substrate for Yarrowia lipolytica biological applications. Biomass and Bioenergy, 48, 148–166. DOI: 10.1016/j.biombioe.2012.11.021.

    Article  Google Scholar 

  • Sawada, K., Taki, A., Yamakawa, T., & Seki, M. (2009). Key role for transketolase activity in erythritol production by Trichosporonoides megachiliensis SN-G42. Journal of Bioscience and Bioengineering, 108, 385–390. DOI: 10.1016/j.jbiosc.2009.05.008.

    Article  CAS  Google Scholar 

  • Sugimoto, S., & Shiio, I. (1989). Regulation of enzymes for erythrose 4-phosphate synthesis in Brevibacterium flavum. Agricultural and Biological Chemistry, 53, 2081–2987. DOI: 10.1080/00021369.1989.10869641.

    CAS  Google Scholar 

  • Tomaszewska, L., Rywi´nska, A., & Gładkowski, W. (2012). Production of erythritol and mannitol by Yarrowia lipolytica yeast in media containing glycerol. Journal of Industrial Microbiology & Biotechnology, 39, 1333–1343. DOI: 10.1007/s10295-012-1145-6.

    Article  CAS  Google Scholar 

  • Tomaszewska, L., Rakicka, M., Rymowicz, W., & Rywi´nska, A. (2014). A comparative study on a glicerol metabolism to erythritol and citric acid in Yarrowia lipolytica yeast cells. FEMS Yeast Research, 14, 966–976. DOI: 10.1111/1567-1364.12184.

    Article  CAS  Google Scholar 

  • van Eck, J. H., Prior, B. A., & Brandt, E. V. (1993). The water relations of growth and polyhydroxy alcohol production by ascomycetous yeasts. Journal of General Microbiology, 139, 1047–1054. DOI: 10.1099/00221287-139-5-1047.

    Article  Google Scholar 

  • van Zyl, P. J., Prior, B. A., & Kilian, S. G. (1991). Regulation of glycerol metabolism in Zygosaccharomyces rouxii in response to osmotic stress. Applied Microbiology and Biotechnology, 36, 369–374. DOI: 10.1007/bf00208158.

    Article  Google Scholar 

  • Veiga-Da-Cunha, M., Firme, P., San Romão, M. V., & Santos, H. (1992). Application of 13C nuclear magnetic resonance to elucidate the unexpected biosynthesis of erythritol by Leuconostoc oenos. Applied and Environmental Microbiology, 58, 2271–2279.

    CAS  Google Scholar 

  • White, H. B., & Kaplan, N. O. (1969). Purification and properties of two types of diphosphopyridine nucleotide-linked glycerol 3-phosphate dehydrogenases from chicken breast muscle and chicken liver. Journal of Biological Chemistry, 244, 6031–6039.

    CAS  Google Scholar 

  • Yang, L. B., Zhan, X. B., Zheng, Z. Y., Wu, J. R., Gao, M. J., & Lin, C. C. (2014). A novel osmotic pressure control fed-batch fermentation strategy for improvement of erythritol production by Yarrowia lipolytica from glycerol. Bioresource Technology, 151, 120–127. DOI: 10.1016/j.biortech.2013.10.031.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ludwika Tomaszewska-Hetman.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomaszewska-Hetman, L., Rywi´nska, A. Erythritol biosynthesis from glycerol by Yarrowia lipolytica yeast: effect of osmotic pressure. Chem. Pap. 70, 272–283 (2016). https://doi.org/10.1515/chempap-2015-0201

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/chempap-2015-0201

Navigation