Skip to main content
Log in

Enhancement of Copper Uptake of Yeast Through Systematic Optimization of Medium and the Cultivation Process of Saccharomyces cerevisiae

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

Abstract

Copper is an essential trace element for living organisms. Copper enriched by yeast of Saccharomyces cerevisiae is regarded as the biologically available organic copper supplement with great potentiality for application. However, the lower uptake ratio of copper ions makes the production of copper enriched by yeast uneconomically and environmentally unfriendly. In this study, S. cerevisiae Cu-5 with higher copper tolerance and intracellular copper accumulation was obtained by screening of our yeast strains collection. To increase the uptake ratio of copper ions, the medium composition and cultivation conditions for strain Cu-5 were optimized systematically. A medium comprised of glucose, yeast extract, (NH4)2SO4, and inorganic salts was determined, then a novel cultivation strategy including pH control at 5.5 and increasing amounts of yeast extract for a higher concentration of copper ion in the medium was developed. The uptake ratios of copper ions were more than 90% after combining 50 to 100 mg/L copper ions with 3.5 to 5.0 g/L yeast extract, which is the highest until now and is conducive to the cost-effective and environmentally friendly production of bioactive copper in yeast-enriched form.

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
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The authors declare that the data and materials are transparent.

Code Availability

Not applicable.

References

  1. Richard, A. F., & Dennis, J. T. (2011). Copper: An essential metal in biology. Current Biology, 21, R877-883. https://doi.org/10.1016/j.cub.2011.09.040

    Article  CAS  Google Scholar 

  2. Tapiero, H., Townsen, D. M., & Tew, K. D. (2003). Trace elements in human physiology and pathology. Copper. Biomed Pharmacother, 57, 386–398. https://doi.org/10.1016/s0753-3322(03)00012-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Manzoni, M., Rollini, S. M., & Benedetti, A. (2009). Copper-enriched biomass, method for the preparation thereof and pro-biotic cosmetic, dietary and neutraceutic products comprising the same. Patent PCT/IB2009/053072.2009.

  4. Klevay, L. M. (2000). Dietary copper and risk of coronary heart disease. American Journal of Clinical Nutrition, 71, 1213–1214. https://doi.org/10.1093/ajcn/71.5.1213

    Article  CAS  Google Scholar 

  5. National Research Council (US). (1989). Recommended dietary allowances (10th ed.). National Academy Press.

    Google Scholar 

  6. Leslie, M. K. (1998). Lack of a recommended dietary allowance for copper may be hazardous to your health. Journal of the American College of Nutrition, 17, 322–326. https://doi.org/10.1080/07315724.1998.10718769

    Article  Google Scholar 

  7. Niu, Y., Wang, J., Zhang, C., & Chen, Y. (2017). Rapid determination of trace copper in animal feed based on micro-plate colorimetric reaction and statistical partitioning correction. Food Chemistry, 221, 1406–1414. https://doi.org/10.1016/j.foodchem.2016.11.012

    Article  CAS  PubMed  Google Scholar 

  8. Scott, A., Vadalasetty, K. P., Łukasiewicz, M., Jaworski, S., Wierzbicki, M., Chwalibog, A., & Sawosz, E. (2018). Effect of different levels of copper nanoparticles and copper sulphate on performance, metabolism and blood biochemical profiles in broiler chicken. Journal of Animal Physiology Animal Nutrition, 102, e364–e373. https://doi.org/10.1111/jpn.12754

    Article  CAS  PubMed  Google Scholar 

  9. Cao, H., Su, R., Hu, G., Li, C., Guo, J., Pan, J., & Tang, Z. (2016). In vivo effects of high dietary copper levels on hepatocellular mitochondrial respiration and electron transport chain enzymes in broilers. British Poultry Science, 57, 63–70. https://doi.org/10.1080/00071668.2015.1127895

    Article  CAS  PubMed  Google Scholar 

  10. Leeson, S. (2009). Copper metabolism and dietary needs. Worlds Poultry Science Journal, 65, 353–366. https://doi.org/10.1017/S0043933909000269

    Article  Google Scholar 

  11. Mrvcić, J., Stanzer, D., Stehlik-Tomas, V., Skevin, D., & Grba, S. (2007). Optimization of bioprocess for production of copper-enriched biomass of industrially important microorganism Saccharomyces cerevisiae. Journal of Bioscience Bioengineering, 103, 331–337. https://doi.org/10.1263/jbb.103.331

    Article  CAS  PubMed  Google Scholar 

  12. Świątkiewicz, S., Arczewska-Włosek, A., & Józefiak, D. (2014). The efficacy of organic minerals in poultry nutrition: Review and implications of recent studies. Worlds Poultry Science Journal, 70, 475–486. https://doi.org/10.1017/S0043933914000531

    Article  Google Scholar 

  13. Vesna, S. T., Vlatka, G. Z., Damir, S., Slobodan, G., & Nada, V. (2004). Zinc, copper and manganese enrichment in yeast Saccharomyces cerevisiae. Food Technology Biotechnology, 42, 115–120. https://doi.org/10.1177/1082013204043764

    Article  CAS  Google Scholar 

  14. Wang, L., Song, Y. Y., Cao, P. H., & Zhao, L. M. (2020). Acclimation of copper absorption ability of Candida utilis. Animal Biotechnology, Published online. https://doi.org/10.1080/10495398.2020.1715418

  15. Dönmez, G., & Aksu, Z. (1999). The effect of copper (II) ions on the growth and bioaccumulation properties of some yeasts. Process Biochemistry, 35, 135–142. https://doi.org/10.1016/S0032-9592(99)00044-8

    Article  Google Scholar 

  16. Šillerová, S., Lavová, B., Urminská, D., Poláková, A., Vollmannová, A., & Harangozo, L. (2012). Copper enriched yeast Saccharomyces cerevisiae as a potential supplement in nutrition. Journal of Microbiology Biotechnology Food Science, 1, 696–702.

    Google Scholar 

  17. Mazo, V. K., Gmoshinski, I. V., & Zorin, S. N. (2007). New food sources of essential trace elements produced by biotechnology facilities. Biotechnology Journal, 2, 1297–1305. https://doi.org/10.1002/biot.200700015

    Article  CAS  PubMed  Google Scholar 

  18. Vinson, J. A., Tompkins, T. A., & Agbor, G. A. (2007). Comparative bioavailability of mineral-enriched gluconates and yeast in rat liver after depletion-repletion feeding. Biological Trace Element Research, 118, 104–110. https://doi.org/10.1007/s12011-007-0004-1

    Article  CAS  PubMed  Google Scholar 

  19. Adamo, G. M., Brocca, S., Passolunghi, S., Salvato, B., & Lotti, M. (2012). Laboratory evolution of copper tolerant yeast strains. Microbial Cell Factories, 11, 1–11. https://doi.org/10.1186/1475-2859-11-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Pope, C. R., De Feo, C. J., & Unger, V. M. (2013). Cellular distribution of copper to superoxide dismutase involves scaffolding by membranes. Proceedings of the National Academy of Sciences of the Unite State of America, 110, 20491–20496. https://doi.org/10.1073/pnas.1309820110

    Article  CAS  Google Scholar 

  21. Sun, X. Y., Liu, L. L., Zhao, Y., Ma, T. T., Zhao, F., Huang, W. D., & Zhan, J. C. (2016). Effect of copper stress on growth characteristics and cultivation properties of Saccharomyces cerevisiae and the pathway of copper adsorption during wine cultivation. Food Chemistry, 192, 43–52. https://doi.org/10.1016/j.foodchem.2015.06.107

    Article  CAS  PubMed  Google Scholar 

  22. Smith, A. D., Logeman, B. L., & Thiele, D. J. (2017). Copper acquisition and utilization in fungi. Annual Review of Microbiology, 71, 597–623. https://doi.org/10.1146/annurev-micro-030117-020444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rong-Mullins, X. Q., Winans, M. J., Lee, J. B., Lonergan, Z. R., Pilolli, V. A., Weatherly, L. M., Camenzind, T. W., Jiang, L., Cumming, J. R., Oporto, G. S., & Gallagher, J. E. G. (2017). Proteomic and genetic analysis of Saccharomyces cerevisiae response to soluble copper leads to improvement of antimicrobial function of cellulosic copper nanoparticles. Metallomics, 9, 1304–1315. https://doi.org/10.1039/c7mt00147a

    Article  CAS  PubMed  Google Scholar 

  24. Berterame, N. M., Martani, F., Porro, D., & Branduardi, P. (2018). Copper homeostasis as a target to improve Saccharomyces cerevisiae tolerance to oxidative stress. Metabolic Engineering, 46, 43–50. https://doi.org/10.1016/j.ymben.2018.02.010

    Article  CAS  PubMed  Google Scholar 

  25. Vest, K. E., Wang, J., Gammon, M. G., Maynard, M. K., White, O. L., Cobine, J. A., Mahone, W. K., & Cobine, P. A. (2016). Overlap of copper and iron uptake systems in mitochondria in Saccharomyces cerevisiae. Open Biology, 6, 150223. https://doi.org/10.1098/rsob.150223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lu, Y., Cheng, Y. F., He, X. P., Guo, X. N., & Zhang, B. R. (2012). Improvement of robustness and ethanol production of ethanologenic Saccharomyces cerevisiae under co-stress of heat and inhibitors. Journal of Industrial Microbiology & Biotechnology, 39, 73–80. https://doi.org/10.1007/s10295-011-1001-0

    Article  CAS  Google Scholar 

  27. van Hoek, P., de Hulster, E., van Dijken, J. P., & Pronk, J. T. (2000). Fermentative capacity in high-cell-density fed-batch cultures of baker’s yeast. Biotechnology Bioengineering, 68, 517–523. https://doi.org/10.1002/(SICI)1097-0290

    Article  PubMed  Google Scholar 

  28. Snell, F. D., Snell, C. T., & Snell, C. A. (1959). Colorimetric methods of analysis. D.Van Nostrand Company Inc.

    Book  Google Scholar 

  29. Jones, R. P., & Gadd, G. M. (1990). Ionic nutrition of yeast – physiological mechanisms involved and implications for biotechnology. Enzyme and Microbial Technology, 12, 402–418. https://doi.org/10.1016/0141-0229(90)90051-Q

    Article  CAS  Google Scholar 

  30. Engl, A., & Kunz, B. (1995). Biosorption of heavy metals by Saccharomyces cerevisiae: Effects of nutrient conditions. Journal of Chemical Technology & Biotechnology, 63, 257–261.

    Article  CAS  Google Scholar 

  31. Karamushka, V. I., & Gadd, G. M. (1994). Influence of copper on proton efflux from Saccharomyces cerevisiae and the protective effect of calcium and magnesium. FEMS Microbiology Letters, 122, 33–38. https://doi.org/10.1111/j.1574-6968,1994.tb07139.x

    Article  CAS  PubMed  Google Scholar 

  32. Portnoy, M. E., Schmidt, P. J., Rogers, R. S., & Culotta, V. C. (2001). Metal transporters that contribute copper to metallochaperones in Saccharomyces cerevisiae. Molecular Genetics & Genomics, 265, 873–882. https://doi.org/10.1007/s004380100482

    Article  CAS  Google Scholar 

  33. Cyert, M. S., & Philpott, C. C. (2013). Regulation of cation balance in Saccharomyces cerevisiae. Genetics, 193, 677–713. https://doi.org/10.1534/genetics.112.147207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lin, C. M., Crawford, B. F., & Kosman, D. J. (1993). Distribution of 64Cu in Saccharomyces cerevisiae: Kinetic analyses of partitioning. Journal of General Microbiology, 139, 1617–1626. https://doi.org/10.1099/00221287-139-7-1617

    Article  CAS  PubMed  Google Scholar 

  35. Hughes, M. N., & Poole, R. K. (1991). Metal speciation and microbial growth: the hard (and soft) facts. Journal of General Microbiology, 137, 725–734. https://doi.org/10.1099/00221287-137-4-725

    Article  CAS  Google Scholar 

  36. Sarais, I., Manazno, M., Bertoldi, M. D., Romandini, P., Beltramini, M., Salvato, B., & Rocco, G. P. (1994). Adaptation of a Saccharomyces cerevisiae strain to high copper concentrations. BioMetals, 7, 221–226. https://doi.org/10.1007/BF00149552

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge colleagues from the public technology service center in the Institute of Microbiology, Chinese Academy of Sciences, for their technical assistance. We thank professor Fengyan Bai from the Institute of Microbiology, Chinese Academy of Sciences for providing S. cerevisiae strain S288C.

Funding

This work was financially supported by the National Key R & D Program of China (No. 2018YFD0500605)

Author information

Authors and Affiliations

Authors

Contributions

Xue-Na Guo designed and performed the experiments, processed and interpreted the data, and prepared the manuscript. Xiao-Xian He participated in designing and performing experiments, processing and interpreting data. Li-Bin Zhang, Yan-Fei Cheng, and Xiu-Mei Bai performed the experiments. Zhao-Yue Wang processed and interpreted the data. Xiu-Ping He supervised the experiments and revised the manuscript.

Corresponding author

Correspondence to Xiu-Ping He.

Ethics declarations

Ethics Approval

This article does not contain any studies involving humans and animals.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Xue-Na Guo and Xiao-Xian He contributed equally to this manuscript.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2814 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, XN., He, XX., Zhang, LB. et al. Enhancement of Copper Uptake of Yeast Through Systematic Optimization of Medium and the Cultivation Process of Saccharomyces cerevisiae. Appl Biochem Biotechnol 194, 1857–1870 (2022). https://doi.org/10.1007/s12010-021-03775-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-021-03775-7

Keywords

Navigation