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Yeasts collectively extend the limits of habitable temperatures by secreting glutathione

ABSTRACT: The conventional view is that high temperatures cause microorganisms to replicate slowly or die. In this view, microorganisms autonomously combat heat-induced damage. However, microorganisms co-exist with each other, which raises the underexplored and timely question of whether microorganisms can cooperatively combat heat-induced damages at high temperatures. Here, we use the budding yeast Saccharomyces cerevisiae to show that cells can help each other and their future generations to survive and replicate at high temperatures. As a consequence, even at the same temperature, a yeast population can exponentially grow, never grow or grow after unpredictable durations (hours to days) of stasis, depending on its population density. Through the same mechanism, yeasts collectively delay and can eventually stop their approach to extinction, with higher population densities stopping faster. These features arise from yeasts secreting and extracellularly accumulating glutathione—a ubiquitous heat-damage-preventing antioxidant. We show that the secretion of glutathione, which eliminates harmful extracellular chemicals, is both necessary and sufficient for yeasts to collectively survive at high temperatures. A mathematical model, which is generally applicable to any cells that cooperatively replicate by secreting molecules, recapitulates all of these features. Our study demonstrates how organisms can cooperatively define and extend the boundaries of life-permitting temperatures.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE137151 | GEO | 2020/03/24

REPOSITORIES: GEO

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Project description:This study was conducted to determine the impact of extreme temperatures, aiming at controlling microorganisms by cooking, on the physiology and the transcriptome of Escherichia coli. ABSTRACT: Because the genome of Escherichia coli K12 is well understood, this organism was used as a model to investigate physiological and molecular changes during cell adaptation and survival to cooking temperatures used in the food industry. Bacteria grown at 37Â°C to stationary phase in Brain Heart Infusion (BHI) broth, were heated at 58Â°C or 60Â°C to reach a process lethality value (F) of 2 and 3, or until an internal core temperature of 71Â°C was reached (control cooking temperature). Both growth recovery and cell membrane integrity were evaluated immediately after heating and a global transcription analysis was performed by using gene expression microarrays. Only cells heated at 58Â°C F = 2 were still able to grow on liquid or solid BHI after heat treatment. However, their transcriptome did not differ significantly compared to those of bacteria heated at 58Â°C F = 3 (P-FDR > 0.01) where no growth recovery was observed post treatment. Genome-wide transcriptomic data obtained at 71Â°C were distinct from the other treatments. Quantification of heat-shock genes expression by real-time PCR revealed that dnaK and groEL mRNA levels were significantly lower at 71Â°C than at 58Â°C and 60Â°C (P < 0.0001). Furthermore, despite of similar cell inactivation but growth on BHI media after heating, 132 and 8 genes were differentially expressed at 71Â°C when compared to 58Â°C and 60Â°C at F = 3 respectively (P-FDR < 0.01). Among them, genes like aroA, citE, glyS, oppB and asd, whose expression was up-regulated at 71Â°C, may be considered as good biomarkers to determine more accurately the efficiency of heat treatments. Bacteria were submitted to four different heat-treatments. Biological replicates: 5 Controls grown to an optimal temperature of 37Â°C (and used to prepare a common reference for each array hybridization), 5 Treatment 1 (58Â°C F = 2), 4 Treatment 2 (58Â°C F = 3), 4 Treatment 3 (60Â°C F = 3), 5 Treatment 4 (core temperature of 71Â°C). Treatment replicates were randomly hybridized on 3 microarray slides Agilent 8x15K (total of 24 array areas). Equal amounts of the labeled control cDNA pool and labeled cDNA from one of the heated groups were mixed and hybridized on each array.

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Yeasts collectively extend the limits of habitable temperatures by secreting glutathione

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