Research ArticleMicrobiology

Reduced ATP-dependent proteolysis of functional proteins during nutrient limitation speeds the return of microbes to a growth state

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Science Signaling  26 Jan 2021:
Vol. 14, Issue 667, eabc4235
DOI: 10.1126/scisignal.abc4235

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Protein preservation speeds growth recovery

During nutrient deprivation, microbes cease to rapidly grow and enter stationary phase. Yeom and Groisman found that the decrease in intracellular ATP experienced by Salmonella in stationary phase inhibited the homeostatic degradation of critical proteins that are substrates of ATP-dependent proteases without affecting that of other protein substrates for those proteases. The selective preservation of protease substrates did not depend on the particular nutrient that was limiting, and it enabled Salmonella to rapidly resume exponential growth when the missing nutrient became available. A similar phenomenon was observed in yeast, suggesting that this may be a general mechanism for ensuring that microbes can rapidly recover from starvation.

Abstract

When cells run out of nutrients, the growth rate greatly decreases. Here, we report that microorganisms, such as the bacterium Salmonella enterica serovar Typhimurium, speed up the return to a rapid growth state by preventing the proteolysis of functional proteins by ATP-dependent proteases while in the slow-growth state or stationary phase. This reduction in functional protein degradation resulted from a decrease in the intracellular concentration of ATP that was nonetheless sufficient to allow the continued degradation of nonfunctional proteins by the same proteases. Protein preservation occurred under limiting magnesium, carbon, or nitrogen conditions, indicating that this response was not specific to low availability of a particular nutrient. Nevertheless, the return to rapid growth required proteins that mediate responses to the specific nutrient limitation conditions, because the transcriptional regulator PhoP was necessary for rapid recovery only after magnesium starvation. Reductions in intracellular ATP and in ATP-dependent proteolysis also enabled the yeast Saccharomyces cerevisiae to recover faster from stationary phase. Our findings suggest that protein preservation during a slow-growth state is a conserved microbial strategy that facilitates the return to a growth state once nutrients become available.

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