Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism

<i>Zygosaccharomyces rouxii</i> is a typical aroma-producing yeast in food brewing, but it has low heat resistance and poor proliferation ability at high temperature. Trehalose is generally considered to be a protective agent that helps stable yeast cells resist heat shock stress, but it...

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Main Authors: Xiong Xiao, Quan Liu, Qian Zhang, Zhenzhen Yan, Dongbo Cai, Xin Li
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Journal of Fungi
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Online Access:https://www.mdpi.com/2309-608X/10/12/842
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author Xiong Xiao
Quan Liu
Qian Zhang
Zhenzhen Yan
Dongbo Cai
Xin Li
author_facet Xiong Xiao
Quan Liu
Qian Zhang
Zhenzhen Yan
Dongbo Cai
Xin Li
author_sort Xiong Xiao
collection DOAJ
description <i>Zygosaccharomyces rouxii</i> is a typical aroma-producing yeast in food brewing, but it has low heat resistance and poor proliferation ability at high temperature. Trehalose is generally considered to be a protective agent that helps stable yeast cells resist heat shock stress, but its functional mechanism for yeast cells in the adaptation period under heat stress is unclear. In this study, the physiological metabolism changes, specific gene transcription expression characteristics, and transcriptome differences of <i>Z. rouxii</i> under different carbon sources under high-temperature stress (40 °C) were compared to explore the mechanism of trehalose inducing <i>Z. rouxii</i> to recover and proliferate under high-temperature stress during the adaptation period. The results showed that high concentration of trehalose (20% Tre) could not be used as the main carbon source for the proliferation of <i>Z. rouxii</i> under long-term high-temperature stress, but it helped to maintain the stability of the cell population. The intracellular trehalose of <i>Z. rouxii</i> was mainly derived from the synthesis and metabolism of intracellular glucose, and the extracellular acetic acid concentration showed an upward trend with the improvement of yeast growth. A high concentration of trehalose (20% Tre) can promote the expression of high glucose receptor gene <i>GRT2</i> (12.0-fold) and induce the up-regulation of <i>HSF1</i> (27.1-fold), <i>MSN4</i> (58.9-fold), <i>HXK1</i> (8.3-fold), and other signal transduction protein genes, and the increase of trehalose concentration will maintain the temporal up-regulation of these genes. Transcriptome analysis showed that trehalose concentration and the presence of glucose had a significant effect on the gene expression of <i>Z. rouxii</i> under high-temperature stress. In summary, trehalose assists <i>Z. rouxii</i> in adapting to high temperature by changing gene expression levels, and assists <i>Z. rouxii</i> in absorbing glucose to achieve cell proliferation.
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spelling doaj-art-7d2da89a2e754865a8275e530909a89e2024-12-27T14:33:55ZengMDPI AGJournal of Fungi2309-608X2024-12-01101284210.3390/jof10120842Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering MetabolismXiong Xiao0Quan Liu1Qian Zhang2Zhenzhen Yan3Dongbo Cai4Xin Li5Cooperative Innovation Center of Industrial Fermentation (Ministry of Education and Hubei Province), Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Key Laboratory of Industrial Microbiology, School of Life and Health Sciences, Hubei University of Technology, Wuhan 430068, ChinaCooperative Innovation Center of Industrial Fermentation (Ministry of Education and Hubei Province), Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Key Laboratory of Industrial Microbiology, School of Life and Health Sciences, Hubei University of Technology, Wuhan 430068, ChinaCooperative Innovation Center of Industrial Fermentation (Ministry of Education and Hubei Province), Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Key Laboratory of Industrial Microbiology, School of Life and Health Sciences, Hubei University of Technology, Wuhan 430068, ChinaCooperative Innovation Center of Industrial Fermentation (Ministry of Education and Hubei Province), Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Key Laboratory of Industrial Microbiology, School of Life and Health Sciences, Hubei University of Technology, Wuhan 430068, ChinaState Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan 430068, ChinaCooperative Innovation Center of Industrial Fermentation (Ministry of Education and Hubei Province), Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Key Laboratory of Industrial Microbiology, School of Life and Health Sciences, Hubei University of Technology, Wuhan 430068, China<i>Zygosaccharomyces rouxii</i> is a typical aroma-producing yeast in food brewing, but it has low heat resistance and poor proliferation ability at high temperature. Trehalose is generally considered to be a protective agent that helps stable yeast cells resist heat shock stress, but its functional mechanism for yeast cells in the adaptation period under heat stress is unclear. In this study, the physiological metabolism changes, specific gene transcription expression characteristics, and transcriptome differences of <i>Z. rouxii</i> under different carbon sources under high-temperature stress (40 °C) were compared to explore the mechanism of trehalose inducing <i>Z. rouxii</i> to recover and proliferate under high-temperature stress during the adaptation period. The results showed that high concentration of trehalose (20% Tre) could not be used as the main carbon source for the proliferation of <i>Z. rouxii</i> under long-term high-temperature stress, but it helped to maintain the stability of the cell population. The intracellular trehalose of <i>Z. rouxii</i> was mainly derived from the synthesis and metabolism of intracellular glucose, and the extracellular acetic acid concentration showed an upward trend with the improvement of yeast growth. A high concentration of trehalose (20% Tre) can promote the expression of high glucose receptor gene <i>GRT2</i> (12.0-fold) and induce the up-regulation of <i>HSF1</i> (27.1-fold), <i>MSN4</i> (58.9-fold), <i>HXK1</i> (8.3-fold), and other signal transduction protein genes, and the increase of trehalose concentration will maintain the temporal up-regulation of these genes. Transcriptome analysis showed that trehalose concentration and the presence of glucose had a significant effect on the gene expression of <i>Z. rouxii</i> under high-temperature stress. In summary, trehalose assists <i>Z. rouxii</i> in adapting to high temperature by changing gene expression levels, and assists <i>Z. rouxii</i> in absorbing glucose to achieve cell proliferation.https://www.mdpi.com/2309-608X/10/12/842<i>Zygosaccharomyces rouxii</i>trehalosehigh-temperature adversityproliferationtranscriptome
spellingShingle Xiong Xiao
Quan Liu
Qian Zhang
Zhenzhen Yan
Dongbo Cai
Xin Li
Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism
Journal of Fungi
<i>Zygosaccharomyces rouxii</i>
trehalose
high-temperature adversity
proliferation
transcriptome
title Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism
title_full Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism
title_fullStr Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism
title_full_unstemmed Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism
title_short Exogenous Trehalose Assists <i>Zygosaccharomyces rouxii</i> in Resisting High-Temperature Stress Mainly by Activating Genes Rather than Entering Metabolism
title_sort exogenous trehalose assists i zygosaccharomyces rouxii i in resisting high temperature stress mainly by activating genes rather than entering metabolism
topic <i>Zygosaccharomyces rouxii</i>
trehalose
high-temperature adversity
proliferation
transcriptome
url https://www.mdpi.com/2309-608X/10/12/842
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