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The impact of oxygen availability on yeast survival in stationary phase.

ABSTRACT: Saccharomyces cerevisiae is currently widely used as a model to study chronological aging of metazoan cells. Chronological aging is typically studied in aerobic stationary phase (SP) cultures, i.e. the final stage of batch cultures in which growth is arrested due to exogenous carbon source exhaustion. Survival of yeast cells in SP defines their chronological lifespan (CLS). S. cerevisiae SP cultures have strongly contributed to the understanding of cellular mechanisms involved in aging and indicated a key role for oxygen. Oxygen is the natural starting point for reactive oxygen species (ROS) that may both have malignant and beneficial effects on aging. In addition, oxygen allows yeast to grow on ethanol and organic acids formed during the initial respiro-fermentative growth phase on glucose. This post-diauxic phase is hallmarked by reduced growth rates, increased expression of genes involved in SP survival, and increased stress resistance. To date, the role of oxygen and respiration in aging has mostly been studied using respiratory deficient mutants, and respiration repressing agents. However, genetic or chemical interventions may result in unwanted side effects that influence survival in SP. We therefore followed a different approach to evaluate the impact of oxygen availability on yeast robustness in SP, i.e. its CLS and stress resistance, by using the capability of S. cerevisiae to grow under anaerobic conditions. A thorough physiological comparison of strictly anaerobic and aerobic SP cultures revealed that the presence of oxygen during growth and aging of S. cerevisiae strongly affects its energetic status, longevity and stress tolerance in a positive way. Combining the physiological data with genome-wide expression analysis revealed that the oxygen-dependent diauxic growth phase enabled the full induction of robustness in S. cerevisiae, and points to appropriate pre-conditioning of cells as a crucial factor to survive starvation. These findings highlight the importance of exogenous energy availability in the conditions leading to growth arrest, and bring new insight on the role of oxygen in the aging of eukaryotes.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE69485 | GEO | 2016/01/01

SECONDARY ACCESSION(S): PRJNA285694

REPOSITORIES: GEO

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Project description:Saccharomyces cerevisiae is currently widely used as a model to study chronological aging of metazoan cells. Chronological aging is typically studied in aerobic stationary phase (SP) cultures, i.e. the final stage of batch cultures in which growth is arrested due to exogenous carbon source exhaustion. Survival of yeast cells in SP defines their chronological lifespan (CLS). S. cerevisiae SP cultures have strongly contributed to the understanding of cellular mechanisms involved in aging and indicated a key role for oxygen. Oxygen is the natural starting point for reactive oxygen species (ROS) that may both have malignant and beneficial effects on aging. In addition, oxygen allows yeast to grow on ethanol and organic acids formed during the initial respiro-fermentative growth phase on glucose. This post-diauxic phase is hallmarked by reduced growth rates, increased expression of genes involved in SP survival, and increased stress resistance. To date, the role of oxygen and respiration in aging has mostly been studied using respiratory deficient mutants, and respiration repressing agents. However, genetic or chemical interventions may result in unwanted side effects that influence survival in SP. We therefore followed a different approach to evaluate the impact of oxygen availability on yeast robustness in SP, i.e. its CLS and stress resistance, by using the capability of S. cerevisiae to grow under anaerobic conditions. A thorough physiological comparison of strictly anaerobic and aerobic SP cultures revealed that the presence of oxygen during growth and aging of S. cerevisiae strongly affects its energetic status, longevity and stress tolerance in a positive way. Combining the physiological data with genome-wide expression analysis revealed that the oxygen-dependent diauxic growth phase enabled the full induction of robustness in S. cerevisiae, and points to appropriate pre-conditioning of cells as a crucial factor to survive starvation. These findings highlight the importance of exogenous energy availability in the conditions leading to growth arrest, and bring new insight on the role of oxygen in the aging of eukaryotes. The goal of the present study is to evaluate the impact of oxygen availability on yeast longevity. More specifically, the questions addressed are whether the presence of a â??conditioningâ?? post-diauxic phase and the ability to utilize efficiently reserves, characteristics of aerobicity, affects yeast survival during stationary phase. To this end, S. cerevisiae was cultivated in well controlled bioreactors under the presence or absence of oxygen. S. cerevisiaeâ??s response to oxygen availability was monitored by an in-depth physiological analysis combined with genome wide expression analysis.

Project description:The chronological lifespan (CLS) of Saccharomyces cerevisiae is defined as the number days that non-dividing cells remain viable, typically in stationary phase cultures or in water. CLS is extended by restricting glucose in the starting cultures, and is considered a form of caloric restriction (CR). Through a previous genetic screen our lab determined that deleting components of the de novo purine biosynthesis pathway also significantly increased CLS. Significant similarities in gene expression profiles between calorie restricted WT cells and a non-restricted ade4M-bM-^HM-^F mutant suggested the possibility of common gene expression biomarkers of all chronologically long lived cells that could also provide insights into general mechanisms of lifespan extension. We have identified additional growth conditions that extend CLS of WT cells, including supplementation of the media with isonicotinamide (INAM), a known sirtuin activator, or by supplementation with a concentrate collected from the expired media of a calorie restricted yeast culture, presumably due to an as yet unidentified longevity factor. Using these varied methods to extend CLS, we compared gene expression profiles in the aging cells (at day 8) to identify functionally relevant biomarkers of longevity. Nineteen genes were differentially regulated in all 4 of the long-lived populations relative to wild type. Of these 19 genes, viable haploid deletion mutants were available for 16 of them, and 12 were found to have a significant impact on CLS. Duplicate cultures were grown to saturation in SC media cultures, aged, and then harvested on day 8. The deletion mutant ade4M-bM-^HM-^F as well as WT cells treated with 25 mM isonicotinamide, calorie restricted (0.5% glucose), or treated with expired media concentrate from previously calorie restricted cultures. These 4 conditions were then compared to a wild-type (WT) strain. Total RNA was isolated and used for microarray hybridizations onto Affymetrix Yeast 2.0 Gene arrrays.

Project description:Technological advances now make gene expression analysis feasible in any sequenced organism, and new sequencing methods have greatly accelerated genome sequencing. Here we show that important insights into gene function are possible by comparing gene expression response to genetic and environmental perturbations between related species. We present a gene expression compendium designed for maximal gene expression variation in the sensu stricto yeast Saccharomyces bayanus. While many aspects of gene expression are conserved over the 20 million years of evolution separating S. bayanus from the model yeast S. cerevisiae, we observe regulatory changes, including in galactose metabolism and sporulation. The expression data also allows us to predict the biological roles of genes unique to S. bayanus, leading us to propose a role in oxidative stress response for a group of genes, and also to identify a regulatory network specific to this yeast. This dataset contains 53 experiments as follows: (experiment: number of datasets (number of arrays)) growth at different temperatures: 1 (3) heat shock: 4 (18) ammonium: 1 (6) cadmium: 1 (4) copper: 1 (6) lead: 1 (6) nickel: 1 (5) sulfite toxicity: 1 (6) zinc: 1 (6) ethanol toxicity: 1 (6) sorbitol: 1 (6) bleach: 1 (6) hydrogen peroxide: 3 (17) 2-deoxyglucose: 1 (6) hydroxyurea: 1 (6) lovastatin: 1 (4) MG-132: 1 (5) MMS: 1 (6) rapamycin: 1 (6) tunicamycin: 1 (6) zeocin: 1 (6) chronological aging: 3 (13) diauxic shift: 1 (6) galactose: 5 (38) glycerol: 1 (4) sucrose: 1 (4) auxotroph starvation: 1 (11) nutrient limited chemostat growth: 3 (7) mating type and ploidy: 1 (3) alpha factor: 1 (8) cell cycle: 1 (30) sporulation: 3 (18) strain backgrounds: 1 (4) cross progeny: 1 (22) Tn7 insertions: 1 (27) 555.11 and 670.20 knockout tetrads: 2 (8) Timecourse datasets: heat shock, ammonium, cadmium, copper, lead, nickel, sulfite toxicity, zinc, ethanol toxicity, sorbitol, bleach, hydrogen peroxide, 2-deoxyglucose, hydroxyurea, lovastatin, MG-132, MMS, rapamycin, tunicamycin, zeocin, chronological aging, diauxic shift, galactose, glycerol, sucrose, auxotroph starvation, alpha factor, cell cycle, sporulation Single timepoint datasets: growth at different temperatures, strain backgrounds, cross progeny, Tn7 insertions, nutrient limited chemostat growth, mating type and ploidy, 555.11 and 670.20 knockout tetrads Almost all samples were hybridized versus a common reference prepared from a mixture of RNA from Mat a, Matx, and Mata/x cells sampled in both exponential and stationary phase. Additionally, RNA from stress conditions was included: hydrogen peroxide treatment sampled at 10, 30 and 45 minutes, and heat shock from 25 to 37 degrees sampled at 10 and 30 minutes. Samples from the following datasets were not hybridized versus the common reference (reference used in parenthesis and in array annotations): cell cycle (asynchronous culture), constant temperatures (log phase culture), mating type and ploidy (log phase culture), diauxic shift (log phase culture), and strain backgrounds (log phase culture). Replicates and dye swaps were not used.

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The impact of oxygen availability on yeast survival in stationary phase.

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