Bacterial Glycogen Provides Short-Term Benefits in Changing Environments

ABSTRACT

Changing nutritional conditions challenge microbes and shape their evolutionary optimization. Here, we used real-time metabolomics to investigate the role of glycogen in the dynamic physiological adaptation of Escherichia coli to fluctuating nutrients following carbon starvation. After the depletion of environmental glucose, we found significant metabolic activity remaining, which was linked to rapid utilization of intracellular glycogen. Glycogen was depleted by 80% within minutes of glucose starvation and was similarly replenished within minutes of glucose availability. These fast time scales of glycogen utilization correspond to the short-term benefits that glycogen provided to cells undergoing various physiological transitions. Cells capable of utilizing glycogen exhibited shorter lag times than glycogen mutants when starved between periods of exposure to different carbon sources. The ability to utilize glycogen was also important for the transition between planktonic and biofilm lifestyles and enabled increased glucose uptake during pulses of limited glucose availability. While wild-type and mutant strains exhibited comparable growth rates in steady environments, mutants deficient in glycogen utilization grew more poorly in environments that fluctuated on minute scales between carbon availability and starvation. Taken together, these results highlight an underappreciated role of glycogen in rapidly providing carbon and energy in changing environments, thereby increasing survival and competition capabilities under fluctuating and nutrient-poor conditions.

IMPORTANCE Nothing is constant in life, and microbes in particular have to adapt to frequent and rapid environmental changes. Here, we used real-time metabolomics and single-cell imaging to demonstrate that the internal storage polymer glycogen plays a crucial role in such dynamic adaptations. Glycogen is depleted within minutes of glucose starvation and similarly is replenished within minutes of glucose availability. Cells capable of utilizing glycogen exhibited shorter lag times than glycogen mutants when starved between periods of exposure to different carbon sources. While wild-type and mutant strains exhibited comparable growth rates in steady environments, mutants deficient in glycogen utilization grew more poorly in environments that fluctuated on minute scales between carbon availability and starvation. These results highlight an underappreciated role of glycogen in rapidly providing carbon and energy in changing environments, thereby increasing survival and competition capabilities under fluctuating and nutrient-poor conditions.