Diversification of single-cell growth dynamics under starvation influences subsequent reproduction in a clonal bacterial population

Most of the microbes in nature infrequently receive nutrients and are thus in slow- or non-growing states. How quickly they can resume their growth upon an influx of new resources is crucial to occupy environmental niches. Isogenic microbial populations are known to harbor only a fraction of cells with rapid growth resumption, yet little is known about the physiological characteristics of those cells and their emergence in the population. Here, we tracked growth of individual Escherichia coli cells in populations under fluctuating nutrient conditions. We found that shifting from high- to low-nutrient conditions caused stalling of cell growth with few cells continuing to divide extremely slowly, a process which was dependent on lipid turnover. Resuming high-nutrient inflow after low-nutrient conditions resulted in cells resuming growth and division, but with different lag times and leading to varying progeny. The history of cell growth during low-nutrient but not high-nutrient conditions was determinant for resumption of growth, which cellular genealogy analysis suggested to originate from inherited physiological differences. Our results demonstrate that cellular growth dynamics become diverse by nutrient limitations, under which a fraction of cells experienced a particular growth history can reproduce progeny with new resources in the future.