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Genome-Wide Identification of Genes Involved in General Acid Stress and Fluoride Toxicity in Saccharomyces cerevisiae

Johnston, Nichole R., Nallur, Sunitha, Gordon, Patricia B., Smith, Kathryn D., Strobel, Scott A.·2020·Frontiers in Microbiology
DOI 10.3389/fmicb.2020.01410PMC PMC7329995
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FIGURE 1 Toxicity of acids in yeast. (A) The toxic range of each acid in inhibiting yeast growth is assessed over 24 h by a liquid growth assay, with increasing concentrations of each acid. Yeast were then exposed to acids at their IC50 concentrations for 4 h, and the (B) intracellular and (C) extracellular pH of the yeast was established using pH-sensitive dye and a pH electrode, respectively. P values are denoted above, and were calculated using Prism software.
FIGURE 1 Toxicity of acids in yeast. (A) The toxic range of each acid in inhibiting yeast growth is assessed over 24 h by a liquid growth assay, with increasing concentrations of each acid. Yeast were then exposed to acids at their IC50 concentrations for 4 h, and the (B) intracellular and (C) extracellular pH of the yeast was established using pH-sensitive dye and a pH electrode, respectively. P values are denoted above, and were calculated using Prism software.CC BY · PubMed Central
FIGURE 2 Venn diagram of overlapping genes. Each circle encompasses the full set of gene deletions resulting in sensitivity to NaF (133 genes, purple), FCCP (204 genes, red), 2,4-DNP (148 genes, yellow), HCl (161 genes, green), or H2SO4 (132 genes, blue). Also noted in the figure is the percent of those genes that do not overlap with any other dataset.
FIGURE 2 Venn diagram of overlapping genes. Each circle encompasses the full set of gene deletions resulting in sensitivity to NaF (133 genes, purple), FCCP (204 genes, red), 2,4-DNP (148 genes, yellow), HCl (161 genes, green), or H2SO4 (132 genes, blue). Also noted in the figure is the percent of those genes that do not overlap with any other dataset.CC BY · PubMed Central
FIGURE 3 Enrichment analysis for the biological processes and molecular functions of genes conferring resistance to (A) NaF, (B) FCCP, (C) 2,4-DNP, (D) HCl, and (E) H2SO4 stress. Enrichment analysis was performed using WebGestalt, and redundant categories were eliminated. The top 30 most enriched pathways are reported above, having at least an enrichment ration value of 2 and a p-value below 0.01. The colors corresponding to the columns are (green) – golgi, (pink) – ion homeostasis, (purple) – mitochondria, (red) – nucleus, (yellow) – protein transporters, (brown) – ribosomes, (blue) – vacuole, (turquoise) – vesicle-mediated transport, and (black) – other.
FIGURE 3 Enrichment analysis for the biological processes and molecular functions of genes conferring resistance to (A) NaF, (B) FCCP, (C) 2,4-DNP, (D) HCl, and (E) H2SO4 stress. Enrichment analysis was performed using WebGestalt, and redundant categories were eliminated. The top 30 most enriched pathways are reported above, having at least an enrichment ration value of 2 and a p-value below 0.01. The colors corresponding to the columns are (green) – golgi, (pink) – ion homeostasis, (purple) – mitochondria, (red) – nucleus, (yellow) – protein transporters, (brown) – ribosomes, (blue) – vacuole, (turquoise) – vesicle-mediated transport, and (black) – other.CC BY · PubMed Central
FIGURE 4 Cellular components involved in resistance to (A) NaF, (B) FCCP, (C) 2,4-DNP, (D) HCl, and (E) H2SO4 stress. Images were composed using ClueGO software from pathways with pV ≤ 0.050. Node size is proportional to the fraction of genes in that particular node.
FIGURE 4 Cellular components involved in resistance to (A) NaF, (B) FCCP, (C) 2,4-DNP, (D) HCl, and (E) H2SO4 stress. Images were composed using ClueGO software from pathways with pV ≤ 0.050. Node size is proportional to the fraction of genes in that particular node.CC BY · PubMed Central
FIGURE 5 Sensitivity of ΔVMA11 mutation in yeast. (A) Serial dilutions of wild type and ΔVMA11 yeast on agar plates containing normal YPD, and YPD with NaF, HCl, FCCP, CH3COOH, and H2SO4. The IC50’s of each were calculated using the 24-h liquid growth assay (data not shown). (B) Imaging of vacuolar membrane using FM4-64 dye. Cells are grown to log phase. (C) Intracellular pH of wild type and ΔVMA11 yeast after 4 h of growth, as assessed using 5(6)-CFDA. P-value is shown; p-value was calculated using GraphPad Prism Software. (D) Change in reactive oxygenated species production in yeast grown 6 h, in YPD or YPD with acids. Astericks represent statistical significance, as calculated using prism software. Gray asterisks represent the comparison between untreated and acid treated wild type cells, while black asterisks represent the statistical significance between acid treated wild type, and acid treated ΔVMA11 yeast cells.
FIGURE 5 Sensitivity of ΔVMA11 mutation in yeast. (A) Serial dilutions of wild type and ΔVMA11 yeast on agar plates containing normal YPD, and YPD with NaF, HCl, FCCP, CH3COOH, and H2SO4. The IC50’s of each were calculated using the 24-h liquid growth assay (data not shown). (B) Imaging of vacuolar membrane using FM4-64 dye. Cells are grown to log phase. (C) Intracellular pH of wild type and ΔVMA11 yeast after 4 h of growth, as assessed using 5(6)-CFDA. P-value is shown; p-value was calculated using GraphPad Prism Software. (D) Change in reactive oxygenated species production in yeast grown 6 h, in YPD or YPD with acids. Astericks represent statistical significance, as calculated using prism software. Gray asterisks represent the comparison between untreated and acid treated wild type cells, while black asterisks represent the statistical significance between acid treated wild type, and acid treated ΔVMA11 yeast cells.CC BY · PubMed Central
FIGURE 6 Role of endocytosis, vesicle trafficking and V-ATPase in nutrient uptake. Glucose uptake (monitored using the fluorescent dye 2-NBDG) after 4 h exposure to acids in wild type (WT) and (A) endocytosis and vesicle trafficking knockouts and (B) V-ATPase subunit knockouts. (C) 31P NMR of wild type and ΔVMA11 yeast. Statistical significance analysis for (A) had p < 0.0001 for every value of acid treatment compared to wild type, or acid treatment of wild type compared with genetic knockouts. The only exception for this was ΔRVS161 yeast, which had p < 0.001 difference in sugar uptake compared with wild type. Statistical analysis for (B) is represented in the graph, whereby gray asterisks represent the comparison between untreated and acid treated wild type cells, while black asterisks represent the statistical significance between acid treated wild type, and acid treated V-ATPase knockout yeast cells.
FIGURE 6 Role of endocytosis, vesicle trafficking and V-ATPase in nutrient uptake. Glucose uptake (monitored using the fluorescent dye 2-NBDG) after 4 h exposure to acids in wild type (WT) and (A) endocytosis and vesicle trafficking knockouts and (B) V-ATPase subunit knockouts. (C) 31P NMR of wild type and ΔVMA11 yeast. Statistical significance analysis for (A) had p < 0.0001 for every value of acid treatment compared to wild type, or acid treatment of wild type compared with genetic knockouts. The only exception for this was ΔRVS161 yeast, which had p < 0.001 difference in sugar uptake compared with wild type. Statistical analysis for (B) is represented in the graph, whereby gray asterisks represent the comparison between untreated and acid treated wild type cells, while black asterisks represent the statistical significance between acid treated wild type, and acid treated V-ATPase knockout yeast cells.CC BY · PubMed Central

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Metadata

Authors
Johnston, N. R., Nallur, S., Gordon, P. B., Smith, K. D., & Strobel, S. A.
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2020-06-25
Volume
11
ISSN
1664-302X
DOI
10.3389/fmicb.2020.01410
PMC
PMC7329995
Cited by
18
References
1
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
National Institutes of Health

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Johnston, N. R., Nallur, S., Gordon, P. B., Smith, K. D., & Strobel, S. A. (2020). Genome-Wide Identification of Genes Involved in General Acid Stress and Fluoride Toxicity in Saccharomyces cerevisiae. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2020.01410