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.

Glycogen Metabolism Impairment via Single Gene Mutation in the glgBXCAP Operon Alters the Survival Rate of Escherichia coli Under Various Environmental Stresses

“…In this study, we investigated the influences of glycogen on the survival abilities of E. coli BW25113 and its single-gene mutants under starvation, low temperature, desiccation, and oxidative stress. As an important energy reserve, bacterial glycogen was able to provide both short-term benefits in changing environments (Sekar et al, 2020) and long-term persistence in the environment (Bourassa and Camilli, 2009). Our study further confirmed that glycogen over-accumulating strains survived much better than wild-type and other mutated strains under starvation conditions, even though glycogen utilization was disrupted.…”

Metabolism of non-growing bacteria

“…Especially, the short-term storage compound glycogen seems to be important to maintain metabolic activity directly after removal of a carbon source. This result was supported by a study that used metabonomics to compare metabolism of wild-type E. coli and a glycogen deficient mutant (Sekar et al 2020). The study showed that glycogen utilization plays an important role in providing energy during the very early phase of carbon starvation and that this enabled non-growing E. coli to quickly resume growth when glucose became available.…”

Probiogenomics Analysis of 97 Lactobacillus crispatus Strains as a Tool for the Identification of Promising Next-Generation Probiotics

“…Furthermore, the genome of LB57 encodes 33 genes classified as GT3, absent in the other isolates, involved in glycogen synthesis ( Figure 4 ). This may indicate that this strain has evolved to use glycogen for energy reserve, as previously observed in other bacteria, resulting in higher resistance to starvation and improved ecological fitness [ 12 , 36 ]. GT3 genes have been previously observed in L. crispatus strains isolated from vaginal microbial populations characterized by lactobacilli dominance [ 12 ].…”