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

The ability to survive starvation is an integral part of bacterial fitness and determines composition, turnover and biodiversity in microbial ecosystems. Starving bacteria enter a state known as plasmolysis in which their cytoplasm contracts from the cell wall. Plasmolysis is often thought to be a pathological, passive condition, arising automatically from the lack of ATP. Here we show that contrary to this notion, maintaining plasmolysis is an active, ATP-consuming state that is essential for starvation survival. We show that ion homeostasis to maintain plasmolysis consumes the largest part of the energy budget of starving cells and directly determines death rates in starvation. Our mathematical model accurately predicts death rates for various 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 the species.