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A Hierarchical Transcriptional Regulatory Network Required for Long-Term Thermal Stress Tolerance in an Industrial Saccharomyces cerevisiae Strain

ABSTRACT: Yeast cells suffer from continuous and long-term thermal stress during high-temperature ethanol fermentation. Understanding the mechanism of yeast thermotolerance is important not only for studying microbial stress biology in basic research but also for developing thermotolerant strains for industrial application. Here, we compared the effects of 23 transcription factor (TF) deletions on high-temperature ethanol fermentation and cell survival after heat shock treatment and identified three core TFs, Sin3p, Srb2p and Mig1p, that are involved in regulating the response to long-term thermotolerance. Further analyses of comparative transcriptome profiling of the core TF deletions and transcription regulatory associations revealed a hierarchical transcriptional regulatory network centered on these three TFs. This global transcriptional regulatory network provided a better understanding of the regulatory mechanism behind long-term thermal stress tolerance as well as potential targets for transcriptome engineering to improve the performance of high-temperature ethanol fermentation by an industrial Saccharomyces cerevisiae strain.

SUBMITTER: Gan Y

PROVIDER: S-EPMC8804346 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:spt23 plays multiple roles in the thermal tolerance of budding yeast. spt23 regulates unsaturated lipid acid (ULA) content in the cell, which can then significantly affect cellular thermal tolerance. Being a Ty suppressor, spt23 can also interact with transposons (Tys) that are contributors to yeast's adaptive evolution. Nevertheless, few studies have investigated whether and how much spt23 can exert its regulatory functions through transposons. In this study, expression quantitative trait loci (eQTL) analysis was conducted with thermal-tolerant Saccharomyces cerevisiae strains, and spt23 was identified as one of the most important genes in mutants. spt23-overexpression (OE), deletion (Del), and integrative-expressed (IE) strains were constructed. Their heat tolerance, ethanol production, the expression level of key genes, and lipid acid contents in the cell membranes were measured. Furthermore, LTR (long terminal repeat)-amplicon sequencing was used to profile yeast transposon activities in the treatments. The results showed the Del type had a higher survival rate, biomass, and ethanol production, revealing negative correlations between spt23 expression levels and thermal tolerance. Total unsaturated lipid acid (TULA) contents in cell membranes were lower in the Del type, indicating its negative association with spt23 expression levels. The Del type resulted in the lower richness and higher evenness in LTR distributions, as well as higher transposon activities. The intersection of 3 gene sets and regression analysis revealed the relative weight of spt23's direct and TY-induced influence is about 4:3. These results suggested a heat tolerance model in which spt23 increases cell thermal tolerance through transcriptional regulation in addition to spt23-transposon triggered unknown responses. KEY POINTS: • spt23 is a key gene for heat tolerance, important for LA contents but not vital. • Deletion of spt23 decreases in yeast's LTR richness but not in evenness. • The relative weight of spt23's direct and TY-induced influence is about 4:3.

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A Hierarchical Transcriptional Regulatory Network Required for Long-Term Thermal Stress Tolerance in an Industrial Saccharomyces cerevisiae Strain

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