Xue-Na Guo: CAS Key Laboratory of Microbial Physiological and Metabolic Engineering, State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.
Xiao-Xian He: CAS Key Laboratory of Microbial Physiological and Metabolic Engineering, State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.
Li-Bin Zhang: State Key Laboratory of Direct-Fed Microbial Engineering, Beijing DaBeiNong Science and Technology Group Co., Ltd. (DBN), Beijing, 100192, China.
Yan-Fei Cheng: CAS Key Laboratory of Microbial Physiological and Metabolic Engineering, State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.
Xiu-Mei Bai: State Key Laboratory of Direct-Fed Microbial Engineering, Beijing DaBeiNong Science and Technology Group Co., Ltd. (DBN), Beijing, 100192, China.
Zhao-Yue Wang: CAS Key Laboratory of Microbial Physiological and Metabolic Engineering, State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.
Xiu-Ping He: CAS Key Laboratory of Microbial Physiological and Metabolic Engineering, State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China. hexp@im.ac.cn. ORCID
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, (NH)SO, 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.
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
[DOI: 10.1016/j.cub.2011.09.040]
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
[DOI: 10.1016/s0753-3322(03)00012-x]
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.
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
[DOI: 10.1093/ajcn/71.5.1213]
National Research Council (US). (1989). Recommended dietary allowances (10th ed.). National Academy Press.
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
[DOI: 10.1080/07315724.1998.10718769]
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
[DOI: 10.1016/j.foodchem.2016.11.012]
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
[DOI: 10.1111/jpn.12754]
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
[DOI: 10.1080/00071668.2015.1127895]
Leeson, S. (2009). Copper metabolism and dietary needs. Worlds Poultry Science Journal, 65, 353–366. https://doi.org/10.1017/S0043933909000269
[DOI: 10.1017/S0043933909000269]
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
[DOI: 10.1263/jbb.103.331]
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
[DOI: 10.1017/S0043933914000531]
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
[DOI: 10.1177/1082013204043764]
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
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
[DOI: 10.1016/S0032-9592(99)00044-8]
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.
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
[DOI: 10.1002/biot.200700015]
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
[DOI: 10.1007/s12011-007-0004-1]
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
[DOI: 10.1186/1475-2859-11-1]
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
[DOI: 10.1073/pnas.1309820110]
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
[DOI: 10.1016/j.foodchem.2015.06.107]
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
[DOI: 10.1146/annurev-micro-030117-020444]
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
[DOI: 10.1039/c7mt00147a]
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
[DOI: 10.1016/j.ymben.2018.02.010]
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
[DOI: 10.1098/rsob.150223]
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
[DOI: 10.1007/s10295-011-1001-0]
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
[DOI: 10.1002/(SICI)1097-0290]
Snell, F. D., Snell, C. T., & Snell, C. A. (1959). Colorimetric methods of analysis. D.Van Nostrand Company Inc.
[DOI: 10.1097/00010694-195907000-00018]
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
[DOI: 10.1016/0141-0229(90)90051-Q]
Engl, A., & Kunz, B. (1995). Biosorption of heavy metals by Saccharomyces cerevisiae: Effects of nutrient conditions. Journal of Chemical Technology & Biotechnology, 63, 257–261.
[DOI: 10.1002/jctb.280630310]
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
[DOI: 10.1111/j.1574-6968,1994.tb07139.x]
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
[DOI: 10.1007/s004380100482]
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
[DOI: 10.1534/genetics.112.147207]
Lin, C. M., Crawford, B. F., & Kosman, D. J. (1993). Distribution of Cu in Saccharomyces cerevisiae: Kinetic analyses of partitioning. Journal of General Microbiology, 139, 1617–1626. https://doi.org/10.1099/00221287-139-7-1617
[DOI: 10.1099/00221287-139-7-1617]
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
[DOI: 10.1099/00221287-137-4-725]
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
[DOI: 10.1007/BF00149552]
Grants
No. 2018YFD0500605/national key r & d program of china