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Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of Saccharomyces cerevisiae to stress induced by sulfur dioxide.

ABSTRACT: During vinification Saccharomyces cerevisiae cells are frequently exposed to high concentrations of sulfur dioxide (SO₂) that is used to avoid overgrowth of unwanted bacteria or fungi present in the must. Up to now the characterization of the molecular mechanisms by which S. cerevisiae responds and tolerates SO₂ was focused on the role of the sulfite efflux pump Ssu1 and investigation on the involvement of other players has been scarce, especially at a genome-wide level. In this work, we uncovered the essential role of the poorly characterized transcription factor Com2 in tolerance and response of S. cerevisiae to stress induced by SO₂ at the enologically relevant pH of 3.5. Transcriptomic analysis revealed that Com2 controls, directly or indirectly, the expression of more than 80% of the genes activated by SO₂, a percentage much higher than the one that could be attributed to any other stress-responsive transcription factor. Large-scale phenotyping of the yeast haploid mutant collection led to the identification of 50 Com2-targets contributing to the protection against SO₂ including all the genes that compose the sulfate reduction pathway (MET3, MET14, MET16, MET5, MET10) and the majority of the genes required for biosynthesis of lysine (LYS2, LYS21, LYS20, LYS14, LYS4, LYS5, LYS1 and LYS9) or arginine (ARG5,6, ARG4, ARG2, ARG3, ARG7, ARG8, ORT1 and CPA1). Other uncovered determinants of resistance to SO₂ (not under the control of Com2) included genes required for function and assembly of the vacuolar proton pump and enzymes of the antioxidant defense, consistent with the observed cytosolic and mitochondrial accumulation of reactive oxygen species in SO₂-stressed yeast cells.

SUBMITTER: Lage P

PROVIDER: S-EPMC6859422 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of Saccharomyces cerevisiae to stress induced by sulfur dioxide.

Lage Patrícia P Sampaio-Marques Belém B Ludovico Paula P Mira Nuno P NP Mendes-Ferreira Ana A

Microbial cell (Graz, Austria) 20190930 11

During vinification Saccharomyces cerevisiae cells are frequently exposed to high concentrations of sulfur dioxide (SO2) that is used to avoid overgrowth of unwanted bacteria or fungi present in the must. Up to now the characterization of the molecular mechanisms by which S. cerevisiae responds and tolerates SO2 was focused on the role of the sulfite efflux pump Ssu1 and investigation on the involvement of other players has been scarce, especially at a genome- ...[more]

PMID: 31799324

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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.

Dataset Information

Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of Saccharomyces cerevisiae to stress induced by sulfur dioxide.

Publications

Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of <i>Saccharomyces cerevisiae</i> to stress induced by sulfur dioxide.

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