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Comparative Analysis of Oxidative Stress During Aging of Kluyveromyces marxianus in Synthetic and Whey Media

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Abstract

During the aging of yeast culture, Kluyveromyces marxianus undergoes a number of changes in physiology and these changes play a significant role during fermentation. Aged stationary phase cells were found to contain more reactive oxygen species. Additionally, the level of oxidant is counteracted by the antioxidant defense system of the cells. Comparison of 3-day-old culture of K. marxianus with 45-day stationary phase culture represents an increased level of ROS inside the cells. Moreover, a decrease in glutathione content was observed over the set of the incubation period. The increased level of superoxide dismutase (SOD) and catalase also revealed that there is oxidative stress during the long period incubation of the stationary phase cells of K. marxianus. The actual phenomenon of aging in dairy yeast K. marxianus is a complex process, but the present study signifies that role of antioxidant defense system during aging in stationary phase cells of K. marxianus.

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References

  1. Galindo-Leva, L. Á., Hughes, S. R., López-Núñez, J. C., Jarodsky, J. M., Erickson, A., Lindquist, M. R., & Qureshi, N. (2016). Growth, ethanol production, and inulinase activity on various inulin substrates by mutant Kluyveromyces marxianus strains NRRL Y-50798 and NRRL Y-50799. Journal of Indutrial Microbiology and  Biotechnology, 43(7), 927–939.

  2. Laun, P., Pichova, A., Madeo, F., Fuchs, J., Ellinger, A., Kohlwein, S., & Breitenbach, M. (2001). Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Molecular Microbiology, 39(5), 1166–1173.

    Article  CAS  Google Scholar 

  3. Stadtman, E. R., & Berlett, B. S. (1997). Reactive oxygen-mediated protein oxidation in aging and disease. Chemical Research in Toxicology, 10(5), 485–494.

    Article  CAS  Google Scholar 

  4. Cyrne, L., Martins, L., Fernandes, L., & Marinho, H. S. (2003). Regulation of antioxidant enzymes gene expression in the yeast Saccharomyces cerevisiae during stationary phase. Free Radical Biology and Medicine, 34(3), 385–393.

    Article  CAS  Google Scholar 

  5. Mesquita, A., Weinberger, M., Silva, A., Sampaio-Marques, B., Almeida, B., Leão, C., & Ludovico, P. (2010). Caloric restriction or catalase inactivation extends yeast chronological lifespan by inducing H2O2 and superoxide dismutase activity. Proceedings of the National Academy of Sciences, 107(34), 15123–15128.

    Article  CAS  Google Scholar 

  6. Jakubowski, W., Biliński, T., & Bartosz, G. (2000). Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae. Free Radical Biology and Medicine, 28(5), 659–664.

    Article  CAS  Google Scholar 

  7. Favre, C., Aguilar, P. S., & Carrillo, M. C. (2008). Oxidative stress and chronological aging in glycogen-phosphorylase-deleted yeast. Free Radical Biology and Medicine, 45(10), 1446–1456.

    Article  CAS  Google Scholar 

  8. Østergaard, H., Tachibana, C., & Winther, J. R. (2004). Monitoring disulfide bond formation in the eukaryotic cytosol. The Journal of Cell Biology, 166(3), 337–345.

    Article  Google Scholar 

  9. Breitenbach, M., Rinnerthaler, M., Hartl, J., Stincone, A., Vowinckel, J., Breitenbach-Koller, H., & Ralser, M. (2014). Mitochondria in ageing: there is metabolism beyond the ROS. FEMS Yeast Research, 14(1), 198–212.

    Article  CAS  Google Scholar 

  10. Trifunovic, A., & Larsson, N. G. (2008). Mitochondrial dysfunction as a cause of ageing. Journal of Internal Medicine, 263(2), 167–178.

    Article  CAS  Google Scholar 

  11. Burtner, C. R., Murakami, C. J., Kennedy, B. K., & Kaeberlein, M. (2009). A molecular mechanism of chronological aging in yeast. Cell Cycle, 8(8), 1256–1270.

    Article  CAS  Google Scholar 

  12. Kokkiligadda, A., Beniwal, A., Saini, P., & Vij, S. (2016). Utilization of cheese whey using synergistic immobilization of β-galactosidase and Saccharomyces cerevisiae cells in dual matrices. Applied Biochemistry and Biotechnology, 179(8), 1469–1484.

    Article  CAS  Google Scholar 

  13. Rahman, I., Kode, A., & Biswas, S. K. (2006). Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature Protocols, 1(6), 3159–3165.

    Article  CAS  Google Scholar 

  14. Abegg, M. A., Alabarse, P. V. G., Casanova, A., Hoscheid, J., Salomon, T. B., Hackenhaar, F. S., & Benfato, M. S. (2010). Response to oxidative stress in eight pathogenic yeast species of the genus Candida. Mycopathologia, 170(1), 11–20.

    Article  CAS  Google Scholar 

  15. Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 276–287.

    Article  CAS  Google Scholar 

  16. Jakubowski, W., Biliński, T., & Bartosz, G. (1999). Sensitivity of antioxidant-deficient yeast Saccharomyces cerevisiae to peroxynitrite and nitric oxide. Biochimica et Biophysica Acta (BBA)-General Subjects, 1472(1), 395–398.

    Article  CAS  Google Scholar 

  17. Nestelbacher, R., Laun, P., Vondráková, D., Pichová, A., Schüller, C., & Breitenbach, M. (2000). The influence of oxygen toxicity on yeast mother cell-specific aging. Experimental Gerontology, 35(1), 63–70.

    Article  CAS  Google Scholar 

  18. Semchyshyn, H. M., & Lozinska, L. M. (2012). Fructose protects baker's yeast against peroxide stress: potential role of catalase and superoxide dismutase. FEMS Yeast Research, 12(7), 761–773.

    Article  CAS  Google Scholar 

  19. Ribeiro, T. P., Fernandes, C., Melo, K. V., Ferreira, S. S., Lessa, J. A., Franco, R. W., & Horn, A. (2015). Iron, copper, and manganese complexes with in vitro superoxide dismutase and/or catalase activities that keep Saccharomyces cerevisiae cells alive under severe oxidative stress. Free Radical Biology and Medicine, 80, 67–76.

    Article  CAS  Google Scholar 

  20. Grzelak, A., Macierzyńska, E., & Bartosz, G. (2006). Accumulation of oxidative damage during replicative aging of the yeast Saccharomyces cerevisiae. Experimental Gerontology, 41(9), 813–818.

    Article  CAS  Google Scholar 

  21. Ayer, A., Gourlay, C. W., & Dawes, I. W. (2014). Cellular redox homeostasis, reactive oxygen species and replicative ageing in Saccharomyces cerevisiae. FEMS Yeast Research, 14(1), 60–72.

    Article  CAS  Google Scholar 

  22. Ashrafi, K., Sinclair, D., Gordon, J. I., & Guarente, L. (1999). Passage through stationary phase advances replicative aging in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, 96(16), 9100–9105.

    Article  CAS  Google Scholar 

  23. MacLean, M., Harris, N., & Piper, P. W. (2001). Chronological lifespan of stationary phase yeast cells; a model for investigating the factors that might influence the ageing of postmitotic tissues in higher organisms. Yeast, 18(6), 499–509.

    Article  CAS  Google Scholar 

  24. Longo, V. D., & Fabrizio, P. (2002). Visions & reflections. Regulation of longevity and stress resistance: a molecular strategy conserved from yeast to humans? Cellular and Molecular Life Sciences CMLS, 59(6), 903–908.

    Article  CAS  Google Scholar 

  25. Grant, C. M., & Dawes, I. W. (1997). Stationary-phase regulation of the Saccharomyces cerevisiae SOD2 gene is dependent on additive effects of HAP2/3/4/5-and STRE-binding elements. Molecular Microbiology, 23(2), 303–312.

    Article  Google Scholar 

  26. Grant, C. M., Collinson, L. P., Roe, J. H., & Dawes, I. W. (1996). Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Molecular Microbiology, 21(1), 171–179.

    Article  CAS  Google Scholar 

  27. Werner-Washburne, M., Braun, E., Johnston, G. C., & Singer, R. A. (1993). Stationary phase in the yeast Saccharomyces cerevisiae. Microbiological Reviews, 57(2), 383–401.

    CAS  Google Scholar 

  28. Nyström, T. (2005). Role of oxidative carbonylation in protein quality control and senescence. The EMBO Journal, 24(7), 1311–1317.

    Article  Google Scholar 

  29. Oliveira, G. A., Tahara, E. B., Gombert, A. K., Barros, M. H., & Kowaltowski, A. J. (2008). Increased aerobic metabolism is essential for the beneficial effects of caloric restriction on yeast life span. Journal of Bioenergetics and Biomembranes, 40(4), 381–388.

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by National Fund for Basic, Strategic and Frontier Application Research in Agriculture (NFBSFARA) and ICAR-National Dairy Research Institute (NDRI), India for providing the necessary support to carry out this research work.

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Correspondence to Shilpa Vij.

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Saini, P., Beniwal, A. & Vij, S. Comparative Analysis of Oxidative Stress During Aging of Kluyveromyces marxianus in Synthetic and Whey Media. Appl Biochem Biotechnol 183, 348–361 (2017). https://doi.org/10.1007/s12010-017-2449-9

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  • DOI: https://doi.org/10.1007/s12010-017-2449-9

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