Cells reshape habitability of temperature by secreting antioxidants to help each other replicate and avoid population extinction

Abstract

SUMMARY How the rising global temperatures affect organisms is a timely question. The conventional view is that high temperatures cause microbes to replicate slowly or die, both autonomously. Yet, microbes co-exist as a population, raising an underexplored question of whether they can cooperatively combat rising temperatures. Here we show that at high temperatures, budding yeasts help each other and future generations of cells replicate by secreting and extracellularly accumulating glutathione - a ubiquitous heat-damage-reducing antioxidant. Yeasts thereby collectively delay and can halt population extinctions at high temperatures. As a surprising consequence, even for the same temperature, a yeast population can either exponentially grow, never grow, or grow after unpredictable durations (hours-to-days) of stasis, depending on its population density. Furthermore, reducing superfluous expression of one gene can extend life-permitting temperature by several Celsius, thereby restoring population growths. Despite theory stating that heat-shocked cells autonomously die, non-growing populations at high temperatures - due to cells cooperating via glutathione - continuously decelerate and can eventually stop their approach to extinction, with higher population-densities stopping faster. A mathematical model recapitulates all these features. These results show how cells can collectively extend boundaries of life-permitting temperatures.