Yeasts collectively extend the limits of habitable temperatures by secreting glutathione

• Published in: Nature microbiology Vol. 5; no. 7; pp. 943 - 954
• Main Authors: Laman Trip, Diederik S, Youk, Hyun
• Format: Journal Article
• Language: English
• Published: England Nature Publishing Group 01.07.2020
• Subjects: Antioxidants; Biological Transport; Cell Proliferation; Ecosystem; Gene Expression Regulation, Fungal; Genes, Fungal; Glutathione; Glutathione - biosynthesis; Heat; High temperature; Mathematical models; Microorganisms; Models, Theoretical; Population density; Saccharomyces cerevisiae; Species extinction; Temperature; Yeast; Yeasts - metabolism
• DOI: 10.1038/s41564-020-0704-2
• ISSN: 2058-5276

The conventional view is that high temperatures cause microorganisms to replicate slowly or die. In this view, microorganisms autonomously combat heat-induced damages. 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.