Survival dynamics of starving bacteria are determined by ion homeostasis that maintains plasmolysis

Abstract

The ability to survive starvation is an integral part of bacterial fitness and determines composition, turn-over and biodiversity in microbial ecosystems. Starving bacteria enter a state, in which their cytoplasm is contracted from the cell wall, known as plasmolysis. Plasmolysis is often thought to be a pathological, passive condition, arising automatically from the lack of ATP. Here, we show that contrary to this existing notion, maintaining plasmolysis is an active, ATP-consuming state that is essential for starvation survival. We show that ion homeostasis for maintaining plasmolysis consumes the lion’s share of starving cells’ energy budget and directly determines death rates in starvation. A quantitative mathematical model accurately predicts death rates across diverse starvation conditions and perturbations. This enabled the development of an optimized starvation medium that would be ideally suited for preserving and transplanting natural microbial communities by maintaining viability but preventing outgrowth of a subset of species.