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Exogenous Thiamine Application Improves the Survival of Wickerhamomyces anomalus under Ethanol Stress

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Abstract

All living organisms require thiamine, a water-soluble vitamin, which is also reported to play a role in response to various abiotic stresses. However, the impact of thiamine on the growth of Wickerhamomyces anomalus under ethanol stress is still not completely understood. In this study, we investigated the effects of exogenous thiamine application on the growth of W. anomalus under ethanol stress. We also investigated how thiamine affected the differentially expressed metabolites (DEMs) using a non-targeted metabolomics approach. The results showed that exogenous thiamine application improved the growth of ethanol-stressed W. anomalus. The DEMs affected by exogenous thiamine application were significantly enriched as ABC transporters process, glycerophospholipid metabolism, purine metabolism, and one carbon pool via folate and sulfur relay system using Kyoto Encyclopedia of Genes and Genomics (KEGG) enrichment analysis. Several pathways, such as arginine biosynthesis, cell cycle, oxidative phosphorylation, etc., were also regulated by thiamine because they were not enriched after exogenous thiamine application. Therefore, thiamine helped to protect W. anomalus from the effects of ethanol stress. These findings offer a theoretical basis for further understanding the regulatory mechanism of thiamine-mediated ethanol stress tolerance in W. anomalus.

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REFERENCES

  1. Abidin, A.Z., Wong, S.Y., Rahman, N.S.A., Idris, Z.H.C., and Yusof, Z.N.B., Osmotic, oxidative and salinity stresses upregulate the expressions of thiamine (vitamin B1) biosynthesis genes (THIC and THI1/THI4) in oil palm (Elaies guineensis), J. Oil Palm Res., 2016, vol. 28, pp. 308–319.

    Article  Google Scholar 

  2. Al-Hakimi, A.B.M. and Hamada, A.M., Ascorbic acid, thiamine, or salicylic acid induced changes in some physiological parameters in wheat grown under copper stress, Plant Protection Sci., 2011, vol. 47, pp. 92–108.

    Article  CAS  Google Scholar 

  3. Alvim, M.C.T., Vital, C.E., Barros, E., Vieira, N.M., Silveira, F.A., Balbino, T.R., Diniz, R.H.S., Brito, A.F., Bazzolli, D.M.S., Ramos, H.J.O., and Silveira, W.B., Ethanol stress responses of Kluyveromyces marxianus CCT 7735 revealed by proteomic and metabolomic analyses, A. van Leeuwenhoek, 2019, vol. 112, pp. 827–845.

    Article  CAS  Google Scholar 

  4. Amjad, S.F., Mansoora, N., Yaseen, S., Kamal, A., Butt, B., Matloob, H., Alamri, S.A.M., Alrumman, S.A., Eid, E.M., and Shahbaz, M., Combined use of endophytic bacteria and pre-sowing treatment of thiamine mitigates the adverse effects of drought stress in wheat (Triticum aestivum L.) cultivars, Sustainability, 2021, vol. 13, p. 6582.

    Article  CAS  Google Scholar 

  5. Auesukaree, C., Molecular mechanisms of the yeast adaptive response and tolerance to stresses encountered during ethanol fermentation, J. Biosci. Bioeng., 2017, vol. 124, pp. 133–142.

    Article  CAS  PubMed  Google Scholar 

  6. Borren, E. and Tian, B., The important contribution of non-Saccharomyces yeasts to the aroma complexity of wine: a review, Foods, 2020, vol. 10, p. 13.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cai, W., Li, B., Chen, Y., Fu, G., Fan, H., Deng, M., Wan, Y., Liu, Na., and Li, M., Increase the content of ester compounds in blueberry wine fermentation with the ester-producing yeast: Candida glabrata, Pichia anomala, and Wickerhamomyces anomalus, Foods, 2022, vol. 11, p. 3655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Canonico, L., Galli, E., Ciani, E., Comitini, F., and Ciani, M., Exploitation of three non-conventional yeast species in the brewing process, Microorganisms, 2019, vol. 7, p. 11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Canonico, L., Solomon, M., Comitini, F., Ciani, M., and Varela, C., Volatile profile of reduced alcohol wines fermented with selected non-Saccharomyces yeasts under different aeration conditions, Food Microbiol., 2019, vol. 84, p. 103247.

    Article  CAS  PubMed  Google Scholar 

  10. Cheng, Y., Du, Z., Zhu, H., Guo, X., and He, X., Protective effects of arginine on Saccharomyces cerevisiae against ethanol stress, Sci. Rep., 2016, vol. 6, pp. 1–12.

    Google Scholar 

  11. Chen, Z., Lin, Y., Zhou, Q., Xiao, S., Li, C., Lin, R., Li, J., Chen, Y., Luo, C., and Mo, Z., Ginsenoside Rg1 mitigates morphine dependence via regulation of gut microbiota, tryptophan metabolism, and serotonergic system function, Biomed. Pharmacother., 2022, vol. 150, p. 112935.

    Article  CAS  PubMed  Google Scholar 

  12. Ducker, G.S. and Rabinowitz, J. D., One-carbon metabolism in health and disease, Cell Metab., 2017, vol. 25, pp. 27–42.

    Article  CAS  PubMed  Google Scholar 

  13. Escribano-Viana, R., González-Arenzana, L., Portu, J., Garijo, P., López-Alfaro, I., López, R., Santamaría, P., and Gutiérrez, A.R., Wine aroma evolution throughout alcoholic fermentation sequentially inoculated with non-Saccharomyces/Saccharomyces yeasts, Food Res. Int., 2018, vol. 112, pp. 17–24.

    Article  CAS  PubMed  Google Scholar 

  14. Fan, G., Teng, C., Xu, D., Fu, Z., Minhazul, K.A.H.M., Wu, Q., Liu, P., Yang, R., and Li, X., Enhanced production of ethyl acetate using co-culture of Wickerhamomyces anomalus and Saccharomyces cerevisiae, J. Biosci. Bioeng., 2019, vol. 128, pp. 564–570.

    Article  CAS  PubMed  Google Scholar 

  15. Fitzpatrick, T.B. and Chapman, L.M., The importance of thiamine (vitamin B1) in plant health: from crop yield to biofortification, J. Biol. Chem., 2020, vol. 295, pp. 12 002–12 013.

    Article  Google Scholar 

  16. Goyer, A., Thiamine in plants: aspects of its metabolism and functions, Phytochemistry, 2010, vol. 7, pp. 1615–1624.

    Article  Google Scholar 

  17. Huang, H.M., Chen, H.L., and Gibson, G.E., Thiamine and oxidants interact to modify cellular calcium stores, Neurochem Res., 2010, vol. 35, pp. 2107–2116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Jing, H., Liu, H., Zhang, L., Gao, J., Song, H., and Tan X., Ethanol induces autophagy regulated by mitochondrial ROS in Saccharomyces cerevisiae, J. Microbiol. Biotechnol., 2018, vol. 28, pp. 1982–1991.

    Article  CAS  PubMed  Google Scholar 

  19. Kaya, C., Aslan, M., Ugurlar, F., and Ashraf, M., Thiamine-induced nitric oxide improves tolerance to boron toxicity in pepper plants by enhancing antioxidants, Turk. J. Agric. For., 2020, vol. 44, pp. 379–390.

    Article  CAS  Google Scholar 

  20. Lin, N., Xu, Y., and Yu, X., Overview of yeast environmental stress response pathways and the development of tolerant yeasts, Systems Microbiol. Biomanufacturing., 2022, vol. 2, pp. 232–245.

    Article  CAS  Google Scholar 

  21. Liu, X., Li, Y., Zhao, H., Yu, Z., Hardie, W.J., and Huang, M., Identification and fermentative properties of an indigenous strain of Wickerhamomyces anomalus isolated from Rosa roxburghii Tratt, Brit. Food J., 2021, vol. 123, pp. 4069–4081.

    Article  Google Scholar 

  22. Li, Y., Long, H., Jiang, G., Gong, X., Yu, Z., Huang, M., Guan, T., Guan, Y., and Liu, X., Analysis of the ethanol stress response mechanism in Wickerhamomyces anomalus based on transcriptomics and metabolomics approaches, BMC Microbiol., 2022, vol. 22, pp. 1–13.

    Article  Google Scholar 

  23. Naheed, R., Zahid, M., Aqeel, M., Maqsood, M.F., Kanwal, H., Khalid, N., Hashem, M., Alamri, S., and Noman, A., Mediation of growth and metabolism of Pisum sativum in salt stress potentially be credited to thiamine, J Soil Sci. Plant Nut., 2022, vol. 22, pp. 1–14.

    Google Scholar 

  24. Padilla, B., Gil, J.V., and Manzanares, P., Challenges of the non-conventional yeast Wickerhamomyces anomalus in winemaking, Fermentation, 2018, vol. 4, p. 68.

    Article  Google Scholar 

  25. Qi, X., Su, X., Guo, H., Qi, J., and Cheng, H., VdThit, a thiamine transport protein, is required for pathogenicity of the vascular pathogen Verticillium dahliae, Mol. Plant Microbe In., 2016, vol. 29, pp. 545–559.

    Article  CAS  Google Scholar 

  26. Rapala-Kozik, M., Kowalska, E., and Ostrowska, K., Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress, J. Exp. Bot., 2008, vol. 59, pp. 4133–4143.

    Article  CAS  PubMed  Google Scholar 

  27. Saini, P., Beniwal, A., Kokkiligadda, A., and Vij, S., Response and tolerance of yeast to changing environmental stress during ethanol fermentation, Process Biochem., 2018, vol. 72, pp. 1–12.

    Article  CAS  Google Scholar 

  28. Stanley, D., Bandara, A., Fraser, S., Chambers, P.J., and Stanley, G.A., The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae, J. Appl. Microbiol., 2010, vol. 109, pp. 13–24.

    Article  CAS  PubMed  Google Scholar 

  29. Sylvander, P., Häubner, N., and Snoeijs, P., The thiamine content of phytoplankton cells is affected by abiotic stress and growth rate, Microb. Ecol., 2013, vol. 65, pp. 566–577.

    Article  CAS  PubMed  Google Scholar 

  30. Takagi, H., Taguchi, J., and Kaino, T., Proline accumulation protects Saccharomyces cerevisiae cells in stationary phase from ethanol stress by reducing reactive oxygen species levels, Yeast, 2016, vol. 33, pp. 355–363.

    Article  CAS  PubMed  Google Scholar 

  31. Tian, S., Liang, X., Chen, J., Zeng, W., Zhou, J., and Du, G., Enhancement of 2-phenylethanol production by a wild-type Wickerhamomyces anomalus strain isolated from rice wine, Bioresource Technol., 2020, vol. 318, p. 124257.

    Article  CAS  Google Scholar 

  32. Vamvakas, S. and Kapolos, J., Factors affecting yeast ethanol tolerance and fermentation efficiency, World J. Microb. Biot., 2020, vol. 36, pp. 1–8.

    Article  Google Scholar 

  33. Wang, W., Fan, G., Li, X., Fu, Z., Liang, X., and Sun, B., Application of Wickerhamomyces anomalus in simulated solid-state fermentation for Baijiu production: changes of microbial community structure and flavor metabolism, Front Microbiol., 2020, vol. 11, p. 598758.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Wang, X., Xu, M., Frank, J. A., Ke, Z., and Luo, J., Thiamine deficiency induces endoplasmic reticulum stress and oxidative stress in human neurons derived from induced pluripotent stem cells, Toxicol. Appl. Pharm., 2017, vol. 320, pp. 26–31.

    Article  CAS  Google Scholar 

  35. Wolak, N., Kowalska, E., Kozik, A., and Rapala-Kozik, M., Thiamine increases the resistance of baker’s yeast Saccharomyces cerevisiae against oxidative, osmotic and thermal stress, through mechanisms partly independent of thiamine diphosphate-bound enzymes, FEMS Yeast Res., 2014, vol. 14, pp. 1249–1262.

    Article  CAS  PubMed  Google Scholar 

  36. Zhao, M., Shi, D., Lu, X., Zong, H., Zhuge, B., and Ji, H., Ethanol fermentation from non-detoxified lignocellulose hydrolysate by a multi-stress tolerant yeast Candida glycerinogenes mutant, Bioresource Technol., 2019, vol. 273, pp. 634–640.

    Article  CAS  Google Scholar 

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Funding

This study was supported by the National Natural Science Foundation of China (32 160 557).

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Authors and Affiliations

  1. College of Food and Pharmaceutical Engineering, Guizhou Institute of Technology, 550003, Guiyang, China

    Y. F. Li, G. L. Jiang, Y. F. Liao, H. Long & X. Z. Liu

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  1. Y. F. Li
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  2. G. L. Jiang
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Correspondence to X. Z. Liu.

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COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest in publishing the article. This article does not contain any studies with human participants or animals performed by any of the authors.

DATA AVAILABILITY STATEMENT

Data will be provided by the corresponding author upon request.

AUTHOR CONTRIBUTION

Contributions to the conception of the work, analysis and writing of manuscript were done by X.L. Analysis and interpretation of data for the work was done by Y.L. (Yinfeng Li), G.J, Y.L and H.L. All authors commented on previous versions of the manuscript. All authors read and approved the final version of the manuscript.

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Li, Y.F., Jiang, G.L., Liao, Y.F. et al. Exogenous Thiamine Application Improves the Survival of Wickerhamomyces anomalus under Ethanol Stress . Microbiology 92, 658–665 (2023). https://doi.org/10.1134/S0026261723601057

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  • DOI: https://doi.org/10.1134/S0026261723601057

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