Advertisement

Microbiology

, Volume 87, Issue 2, pp 173–182 | Cite as

Carbohydrate Spectrum of Extremophilic Yeasts Yarrowia lipolytica under pH Stress

  • V. Yu. Sekova
  • D. I. Dergacheva
  • V. M. Tereshina
  • E. P. Isakova
  • Yu. I. Deryabina
Experimental Articles
  • 40 Downloads

Abstract

Alterations in the concentrations of cell cytosol carbohydrates of polyextremophilic yeasts Yarrowia lipolytica under stresses of diverse nature were observed. Under pH stress, mannitol was the main storage carbohydrate (up to 89% of the total cytosol carbohydrates), while arabitol, glucose, and inositol were present in insignificant amounts (3 to 6%). Experiments with inhibition of de novo mannitol synthesis by bis(p-nitrophenyl) disulfide revealed that the cytoprotective effect of mannitol was most noticeable in the cells grown under acidic conditions (pH 4.0), while the role of catalase and superoxide dismutase, the enzymes of the first line of antioxidant protection, increased under alkaline conditions (pH 9.0). The constitutively high mannitol content in Y. lipolytica cells was hypothesized to be a part of the core mechanism of stress resistance in this yeast species.

Keywords

Yarrowia lipolytica mannitol carbohydrates pH stress oxidative stress antioxidant enzymes 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allocco, J.J., Nare, B., Myers, R.W., Feiglin, M., Schmatz, D.M., and Profous-Juchelka, H., Nitrophenide (Megasul) blocks Eimeria tenella development by inhibiting the mannitol cycle enzyme mannitol-1-phosphate dehydrogenase, J. Parasitol., 2001, vol. 87, pp. 1441–1448.PubMedGoogle Scholar
  2. Aver’yanov, A.A. and Lapikova, V.P., Interaction of sugars with the hydroxyl radical in relation to phytotoxicity of leaf exudates, Biokhimiya, 1989, vol. 54, no. 10, pp. 1646–1651.Google Scholar
  3. Barth, G. and Gaillardin, C., Yarrowia lipolytica, in Nonconventional Yeasts in Biotechnology, Wolf, K., Ed., Berlin: Springer, 1996, pp. 313–388.CrossRefGoogle Scholar
  4. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.CrossRefPubMedGoogle Scholar
  5. Brobst, K.M., Gas–liquid chromatography of trimethylsilyl sugar derivatives, in Metody issledovaniya uglevodov (Methods in Carbohydrate Research), Khorlin, F.Ya., Ed., Moscow: Mir, 1975, pp. 9–13.Google Scholar
  6. Chance, B. and Maehly, A.C., The assay of catalases and peroxidases, Methods Biochem. Anal., 1954, vol. 1, pp. 357–424.PubMedGoogle Scholar
  7. Chaturvedi, V., Batriss, A., and Wong, B., Expression of bacterial mtlD in Saccharomyces cerevisiae results in mannitol synthesis and protects a glycerol-defective mutant from high-salt and oxidative stress, J. Bacteriol., 1997, vol. 79, pp. 157–162.CrossRefGoogle Scholar
  8. Chaturvedi, V., Wong, B., and Newman, S.L., Oxidative killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediate, J. Immunol., 1996, vol. 156, pp. 3836–3840.PubMedGoogle Scholar
  9. Coelho, M.A.Z., Amaral, P.F.F., and Belo, I., Yarrowia lipolytica: an industrial workhorse, in Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, Mendes-Vilas, A., Ed., Bandajos: Formatex RC, 2010, pp. 930–944.Google Scholar
  10. Dutsch, G.A. and Rast, D., Biochemische beziehung zwischen mannitbildung und hexosemonophosphatzyklus in Agaricus bisporus, Phytochemistry. 1972, vol. 11, pp. 2677–2681.CrossRefGoogle Scholar
  11. Eleutherio, E., Panek, A., De Mesquita, J.F., Trevisol, E., and Magalhães, R., Revisiting yeast trehalose metabolism, Curr. Genet., 2015, vol. 61, pp. 263–274.CrossRefPubMedGoogle Scholar
  12. Feofiliva, E.P., Tereshina, V.M., and Gornova, I.B., Alterations in the carbohydrate composition of fungal cells during adaptation to temperature stress, Mikrobiologiya, 1994, vol. 63, no. 5, pp. 792–798.Google Scholar
  13. Feofilova, E.P., Usov, A.I., Mysyakina, I.S., and Kochkina, G.A., Trehalose: chemical structure, biological functions, and practical application, Microbiology (Moscow), 2014, vol. 83, no. 3, pp. 184–194.CrossRefGoogle Scholar
  14. Hörer, S., Stoop, J., Mooibroek, H., Baumann, U., and Sassoon, J., The crystallographic structure of the mannitol 2-dehydrogenase NADP+ binary complex from Agaricus bisporus, J. Biol. Chem., 2001, vol. 276, pp. 27555–27561.CrossRefPubMedGoogle Scholar
  15. Hult, K. and Gatenbeck, S., Production of NADPH in the mannitol cycle and its relation to polyketide formation in Alternaria alternata, Eur. J. Biochem., 1978, vol. 88, pp. 607–612.CrossRefPubMedGoogle Scholar
  16. Hult, K., Veide, A., and Gatenbeck, S., The distribution of the NADPH regenerating mannitol cycle among fungal species, Arch. Microbiol., 1980, vol. 128, pp. 253–255.CrossRefPubMedGoogle Scholar
  17. Ianutsevich E.A., Danilova, O.A., Groza, N.V., and Tereshina, V.M., Membrane lipids and cytosol carbohydrates in Aspergillus niger under osmotic, oxidative, and cold impact, Microbiology (Moscow), 2016, vol. 85, no. 3, pp. 302–310.CrossRefGoogle Scholar
  18. Ianutsevich, E.A., Danilova, O.A., Groza, N.V., Kotlova, E.R., and Tereshina, V.M., Heat shock response of thermophilic fungi: membrane lipids and soluble carbohydrates under elevated temperatures, Microbiology (UK), 2016, vol. 162, no. 6, pp. 989–999.CrossRefGoogle Scholar
  19. Jennings, D.B., Daub, M.E., Pharr, D.M., and Williamson, J.D., Constitutive expression of a celery mannitol dehydrogenase in tobacco enhances resistance to the mannitol-secreting fungal pathogen Alternaria alternata, Plant J., 2002, vol. 32, pp. 41–49.CrossRefPubMedGoogle Scholar
  20. Jennings, D.B., Ehrenshaft, M., Pharr, D.M., and Williamson, J.D., Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 15129–15133.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kayingo, G., Kilian, S.G., and Prior, B.A., Conservation and release of osmolytes by yeasts during hypo-osmotic stress, Arch. Microbiol., 2001, vol. 177, pp. 29–35.CrossRefPubMedGoogle Scholar
  22. Kobayashi, Y., Iwata, H., Yoshida, J., Ogihara, J., Kato, J., and Kasumi, T., Metabolic correlation between polyol and energy-storing carbohydrate under osmotic and oxidative stress condition in Moniliella megachiliensis, J. Biosci. Bioeng., 2015, vol. 120, pp. 405–410.CrossRefPubMedGoogle Scholar
  23. Kostiuk, V.A., Potapovich, A.I., and Kovaleva, Zh.V., A simple and sensitive method of determination of superoxide dismutase activity based on the reaction of quercetin oxidation, Vopr. Med. Khim., 1990 V. 36, no. 2, pp. 88–91.PubMedGoogle Scholar
  24. Liu, H.H., Ji, X.J., and Huang, H., Biotechnological applications of Yarrowia lipolytica: Past, present and future, Biotechnol. Adv., 2015, vol. 33, pp. 1522–1546.CrossRefPubMedGoogle Scholar
  25. Meena, M., Prasad, V., Zehra, A., Gupta, V.K., and Upadhyay, R.S., Mannitol metabolism during pathogenic fungal-host interactions under stressed conditions, Front. Microbiol., 2015, no. 6, p. 1019.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Meng, Q., Zhang, T., Wei, W., Mu, W., and Miao, M., Production of mannitol from a high concentration of glucose by Candida parapsilosis SK26.001, Appl. Biochem. Biotechnol., 2017, vol. 181, pp. 391–406.CrossRefPubMedGoogle Scholar
  27. Nicaud, J.M., Yarrowia lipolytica, Yeast, 2012, vol. 29, pp. 409–418.CrossRefPubMedGoogle Scholar
  28. Patel, T.K. and Williamson, J.D., Mannitol in plants, fungi, and plant-fungal interactions, Trends Plant Sci., 2016, vol. 21, pp. 486–497.CrossRefPubMedGoogle Scholar
  29. Rakicka, M., Rywińska, A., Cybulski K., and Rymowicz W., Enhanced production of erythritol and mannitol by Yarrowia lipolytica in media containing surfactants, Braz. J. Microbiol., 2016, vol. 47, pp. 417–423.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ruijter, G.J.G., Bax, M., Patel, H., Flitter, S.J., van de Vondervoort, P.J., de Vries, R.P., van Kuyk, P.A., and Visser, J., Mannitol is required for stress tolerance in Aspergillus niger conidiospores, Eukaryot. Cell, 2003, vol. 2, pp. 690–698.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Saha, B.C. and Racine, F.M., Biotechnological production of mannitol and its applications, Appl. Microbiol. Biotechnol., 2011, vol. 89, pp. 879–891.CrossRefPubMedGoogle Scholar
  32. Sánchez-Fresneda, R., Guirao-Abad, J.P., Argüelles, A., González-Párraga, P., Valentín, E., and Argüelles, J.C., Specific stress-induced storage of trehalose, glycerol and D-arabitol in response to oxidative and osmotic stress in Candida albicans, Biochem. Biophys. Res. Commun., 2013, vol. 430, no. 4, pp. 1334−1339.CrossRefPubMedGoogle Scholar
  33. Sekova V.Y., Gessler N.N., Isakova E.P., Antipov A.N., Dergacheva D.I., Deryabina Y.I., and Trubnikova E.V., Redox status of extremophilic yeast Yarrowia lipolytica during adaptation to pH-stress, Appl. Biochem. Microbiol., 2015, vol. 51, pp. 649–654.CrossRefGoogle Scholar
  34. Sekova, V.Yu. and Klemeshova, I.S., The mannitol cycle plays and important role in the adaptation of Yarrowia lipolytica yeasts to low ambient pH, Proc. 10th Youth Conf. Int. Particip “Urgent Aspects of Modern Microbiology,” Moscow: Fed. Res. Center Biotechnol., 2015, pp. 136–138.Google Scholar
  35. Smirnoff, N. and Cumbes, Q.J., Hydroxyl radical scavenging activity of compatible solutes, Phytochemistry, 1989, vol. 28, pp. 1057–1060.CrossRefGoogle Scholar
  36. Smolyaniuk, E.V., Bilanrenko, E.N., Tereshina, V.M., Kachalkin, A.V., and Kamzolkina, O.V., Effect of sodium chloride concentration in the medium on the composition of the membrane lipids and carbohydrates in the cytosol of the fungus Fusarium sp., Microbiology (Moscow), 2013, vol. 82, no. 5, pp. 600–608.CrossRefGoogle Scholar
  37. Solomon, P.S., Waters, O.D., and Oliver, R.P., Decoding the mannitol enigma in filamentous fungi, Trends Microbiol., 2007, vol. 15, pp. 257–262.CrossRefPubMedGoogle Scholar
  38. Somogyi, M., Determination of blood sugar, J. Biol. Chem., 1945, vol. 160, pp. 69–73.Google Scholar
  39. Song, S.H. and Vieille, C., Recent advances in the biological production of mannitol, Appl. Microbiol. Biotechnol., 2009, vol. 84, pp. 55–62.CrossRefPubMedGoogle Scholar
  40. Stoop, J.M. and Mooibroek, H., Cloning and characterization of NADP-mannitol dehydrogenase cDNA from the button mushroom, Agaricus bisporus, and its expression in response to NaCl stress, Appl. Environ. Microbiol., 1998, vol. 64, pp. 4689–4696.Google Scholar
  41. Tereshina, V.M., Memorskaia, A.S., and Kotlova, E.R., The effect of different heat influences on composition of membrane lipids and cytosol carbohydrates in mycelial fungi, Microbiology (Moscow), 2011, vol. 80, no. 4, pp. 455–460.CrossRefGoogle Scholar
  42. Tereshina, V.M., Memorskaia, A.S., Kotlova, E.R., and Feofilova, E.P., Composition of membrane lipids and cytosol carbohydrates in Aspergillus niger during heat shock, Microbiology (Moscow), 2010, vol. 79, no. 1, pp. 34–39.CrossRefGoogle Scholar
  43. Tomaszewska, L., Rymowicz, W., and Rywińska, A., Mineral supplementation increases erythrose reductase activity in erythritol biosynthesis from glycerol by Yarrowia lipolytica, Appl. Biochem. Biotechnol., 2014, vol. 172, pp. 3069–3078.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Tomaszewska, L., Rywińska, A., and Gładkowski, W., Production of erythritol and mannitol by Yarrowia lipolytica yeast in media containing glycerol, J. Ind. Microbiol. Biotechnol., 2012, vol. 39, pp. 1333–1343.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vélëz, H., Glassbrook, N.J., and Daub, M.E., Mannitol metabolism in the phytopathogenic fungus Alternaria alternate, Fungal Genet. Biol., 2007, vol. 44, pp. 258–268.CrossRefPubMedGoogle Scholar
  46. Voegele, R.T., Hahn, M., Lohaus, G., Link, T., Heiser, I., and Mendgen, K., Possible roles for mannitol and mannitol dehydrogenase in the biotrophic plant pathogen Uromyces fabae, Plant Physiol., 2005, vol. 137, pp. 190–198.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Yoshikawa, J., Habe, H., Morita, T., Fukuoka, T., Imura, T., Iwabuchi, H., Uemura, S., Tamura, T., and Kitamoto, D., Production of D-arabitol from raw glycerol by Candida quercitrusa, Appl. Microbiol. Biotechnol., 2014a, vol. 98, pp. 2947–2953.CrossRefPubMedGoogle Scholar
  48. Yoshikawa, J., Habe, H., Morita, T., Fukuoka, T., Imura, T., Iwabuchi, H., Uemura, S., Tamura, T., and Kitamoto, D., Production of mannitol from raw glycerol by Candida azyma, J. Biosci. Bioeng., 2014b, vol. 117, pp. 725–729.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • V. Yu. Sekova
    • 1
  • D. I. Dergacheva
    • 1
  • V. M. Tereshina
    • 2
  • E. P. Isakova
    • 1
  • Yu. I. Deryabina
    • 1
  1. 1.Bach Institute of Biochemistry, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  2. 2.Winogradsky Institute of Microbiology, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia

Personalised recommendations