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Cited by 12Mycotoxins in Agriculture and FoodFungal and yeast genetics researchBacterial Genetics and Biotechnology

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Distinct Transcriptional Changes in Response to Patulin Underlie Toxin Biosorption Differences in Saccharomyces cerevisiae

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Oporto, Christian, Villarroel, Carlos, Tapia, Sebastián, García, Verónica, Cubillos, Francisco·2019·Toxins
DOI 10.3390/toxins11070400PMC PMC6669508
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Abstract

Patulin (4-hydroxy-4H-furo[3,2c]pyran-2[6H]-one) is a mycotoxin produced by a suite of fungi species. Patulin is toxic to humans and is a sporadic contaminant in products that were made from fungi-infected fruits. The baker yeast Saccharomyces cerevisiae (S. cerevisiae) has been shown to decrease patulin levels likely by converting it to the less harmful E-ascladiol, yet this capacity is dependent on the strain utilized. In this study we show that four representative strains of different S. cerevisiae lineages differ in their ability to tolerate and decrease patulin levels in solution, demonstrating that some strains are better suitable for patulin biocontrol. Indeed, we tested the biocontrol capacities of the best patulin-reducer strain (WE) in contaminated apple juice and demonstrated their potential role as an efficient natural biocontrol solution. To investigate the mechanisms behind the differences between strains, we explored transcriptomic changes of the top (WE strain) and worst (WA strain) patulin-biocontroller strains after being exposed to this toxin. Large and significant gene expression differences were found between these two strains, the majority of which represented genes associated with protein biosynthesis, cell wall composition and redox homeostasis. Interestingly, the WE isolate exhibited an overrepresentation of up-regulated genes involved in membrane components, suggesting an active role of the membrane towards patulin detoxification. In contrast, WA upregulated genes were associated with RNA metabolism and ribosome biogenesis, suggesting a patulin impact upon transcription and translation activity. These results suggest that different genotypes of S. cerevisiae encounter different stresses from patulin toxicity and that different rates of detoxification of this toxin might be related with the plasma membrane composition. Altogether, our data demonstrates the different molecular mechanisms in S. cerevisiae strains withstanding patulin exposure and opens new avenues for the selection of new patulin biocontroller strains.

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Figure 1 Patulin (PAT) concentration decreases in PBS medium. (A) Schematic representation of the experiment to determine PAT reduction in PBS by different isolates of S. cerevisiae. (B) The bars indicate the percentage of decrease in PAT concentration by isolates of the North American (NA), Wine/European (WE), Sake (SA) and West African (WA) lineages. Isolates were incubated in PBS. PAT was added to the medium prior to the incubation with live cells. Percentages are relative to the control, which was not treated with yeast cells. Letters indicate significant differences among strains (ANOVA, p-value < 0.05). Error bars show the standard error (n = 5).
Figure 1 Patulin (PAT) concentration decreases in PBS medium. (A) Schematic representation of the experiment to determine PAT reduction in PBS by different isolates of S. cerevisiae. (B) The bars indicate the percentage of decrease in PAT concentration by isolates of the North American (NA), Wine/European (WE), Sake (SA) and West African (WA) lineages. Isolates were incubated in PBS. PAT was added to the medium prior to the incubation with live cells. Percentages are relative to the control, which was not treated with yeast cells. Letters indicate significant differences among strains (ANOVA, p-value < 0.05). Error bars show the standard error (n = 5).CC BY · PubMed Central
Figure 2 Effect of PAT on the fitness of WA and WE S. cerevisiae strains. (A) Growth curves of isolates WE (black) and WA (grey) lineages. Isolates were grown in Yeast Extract, Peptone, Dextrose media (YPD) as control (n = 2) and YPD supplemented with 100 µg/mL of PAT (n = 3). (B) Increment on the duration of the lag phase of isolates corresponding to the WE and WA lineages grown in presence of 100 µg/mL of PAT. Values are relative to their growth in control condition (YPD). (*) indicates significant differences due to treatment with PAT between strains (Student’s t test, p-value < 0.05). Error bars indicate the standard deviation (n = 2 and n = 3 in control and PAT treatments, respectively)
Figure 2 Effect of PAT on the fitness of WA and WE S. cerevisiae strains. (A) Growth curves of isolates WE (black) and WA (grey) lineages. Isolates were grown in Yeast Extract, Peptone, Dextrose media (YPD) as control (n = 2) and YPD supplemented with 100 µg/mL of PAT (n = 3). (B) Increment on the duration of the lag phase of isolates corresponding to the WE and WA lineages grown in presence of 100 µg/mL of PAT. Values are relative to their growth in control condition (YPD). (*) indicates significant differences due to treatment with PAT between strains (Student’s t test, p-value < 0.05). Error bars indicate the standard deviation (n = 2 and n = 3 in control and PAT treatments, respectively)CC BY · PubMed Central
Figure 3 PAT reduction by inactive yeast. (A) Schematic representation of the experiment to determine PAT reduction in apple juice by inactive yeast cells. (B) The bars show the percentage of PAT reduction in PBS (n = 4) and in apple juice (n = 9) by inactive cells of the WE isolate. Percentages are relative to the control, which was not treated with yeast cells. Error bars indicate the standard error.
Figure 3 PAT reduction by inactive yeast. (A) Schematic representation of the experiment to determine PAT reduction in apple juice by inactive yeast cells. (B) The bars show the percentage of PAT reduction in PBS (n = 4) and in apple juice (n = 9) by inactive cells of the WE isolate. Percentages are relative to the control, which was not treated with yeast cells. Error bars indicate the standard error.CC BY · PubMed Central
Figure 4 Transcriptome profile of the WE and WA isolates after PAT exposure. (A) A Venn diagram indicating the number of Differentially Expressed Genes (DEGs) upregulated or downregulated in WE and WA strains after incubation of 3 h with PAT. (B,C) Heatmap of hierarchical clustering shows the top 50 most significant genes between untreated and PAT treated WA and WE strains. Red indicates up-regulation and blue indicates down-regulation. Expression values were converted to z-scores and scaled by rows (genes).
Figure 4 Transcriptome profile of the WE and WA isolates after PAT exposure. (A) A Venn diagram indicating the number of Differentially Expressed Genes (DEGs) upregulated or downregulated in WE and WA strains after incubation of 3 h with PAT. (B,C) Heatmap of hierarchical clustering shows the top 50 most significant genes between untreated and PAT treated WA and WE strains. Red indicates up-regulation and blue indicates down-regulation. Expression values were converted to z-scores and scaled by rows (genes).CC BY · PubMed Central
Figure 5 The bar plots show the 5 most enriched GO-terms of the type “Biological Process” in upregulated and downregulated DEGs in the strains WE and WA after PAT exposure. (A) WE Upregulated, (B) WE Down regulated, (C) WA Upregulated and (D) WA Downregulated.
Figure 5 The bar plots show the 5 most enriched GO-terms of the type “Biological Process” in upregulated and downregulated DEGs in the strains WE and WA after PAT exposure. (A) WE Upregulated, (B) WE Down regulated, (C) WA Upregulated and (D) WA Downregulated.CC BY · PubMed Central
Figure 6 Gene-Environment interaction in the response to PAT in WE and WA strains. (A) Number of genes that show a significant (FDR < 0.05) “Genotype” (WE or WA) effect, “Environment” (PAT) effect or Gene and Environment (GxE) interaction effect. (B) Heatmap of hierarchical clustering shows DEGs classified with the GO-term “Cell-wall” exhibiting a “Genotype” effect. Red indicates up-regulation and blue indicates down-regulation. Expression values were converted to z-scores and scaled by rows (genes). (C–E) The five most enriched GO-terms of the type “Biological Process” in upregulated and downregulated genes that show a significant effect in Genotype, Environment and the interaction GxE. For GO-term enrichment of “Genotype” effect genes, we selected those genes which had an absolute fold change greater than 2-fold (706 genes).
Figure 6 Gene-Environment interaction in the response to PAT in WE and WA strains. (A) Number of genes that show a significant (FDR < 0.05) “Genotype” (WE or WA) effect, “Environment” (PAT) effect or Gene and Environment (GxE) interaction effect. (B) Heatmap of hierarchical clustering shows DEGs classified with the GO-term “Cell-wall” exhibiting a “Genotype” effect. Red indicates up-regulation and blue indicates down-regulation. Expression values were converted to z-scores and scaled by rows (genes). (C–E) The five most enriched GO-terms of the type “Biological Process” in upregulated and downregulated genes that show a significant effect in Genotype, Environment and the interaction GxE. For GO-term enrichment of “Genotype” effect genes, we selected those genes which had an absolute fold change greater than 2-fold (706 genes).CC BY · PubMed Central
Figure 7 Differential expression of genes related to sulfur metabolism in response to PAT in WA and WE strains. The heatmaps show the gene expression values which were converted to z-scores and scaled by rows (genes).
Figure 7 Differential expression of genes related to sulfur metabolism in response to PAT in WA and WE strains. The heatmaps show the gene expression values which were converted to z-scores and scaled by rows (genes).CC BY · PubMed Central

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Metadata

Authors
Oporto, C., Villarroel, C., Tapia, S., García, V., & Cubillos, F.
Affiliations
  • Universidad de Santiago de Chile (CL)
  • Millennium Institute for Integrative Biology (CL)
Corresponding author
Cubillos, Francisco
ORCID
Venue
Toxins
Publisher
MDPI AG
Published
2019-07-10
Volume
11
Issue
7
Pages
400
ISSN
2072-6651 (ISSN-L)
DOI
10.3390/toxins11070400
PMC
PMC6669508
OpenAlex
W2956218466
Cited by
12
References
63
Citations by year
2025: 1 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 1
FWCI
1.47
Type
journal article
Language
en
Open access
Licence
Locations
  • Toxins (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Comisión Nacional de Investigación Científica y Tecnológica (FONDECYT 1180161, FONDECYT 3170404, FONDECYT 11140097)
  • Iniciativa Científica Milenio MINECON (Instituto Milenio iBio)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycotoxins in Agriculture and Food
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
patulin, Saccharomyces cerevisiae, detoxification, biological control, transcriptomics, strain differences, plasma membrane composition, redox homeostasis, cell wall composition, ribosome biogenesis, RNA metabolism
MeSH terms
Fruit and Vegetable Juices, RNA-Seq, Food Contamination, Hot Temperature, Patulin, Saccharomyces cerevisiae, Transcription, Genetic, Gene Expression Regulation, Fungal, Malus, Gene-Environment Interaction

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Oporto, C., Villarroel, C., Tapia, S., García, V., & Cubillos, F. (2019). Distinct Transcriptional Changes in Response to Patulin Underlie Toxin Biosorption Differences in Saccharomyces cerevisiae. Toxins. https://doi.org/10.3390/toxins11070400