Density-Dependent Recycling Promotes the Long-Term Survival of Bacterial Populations during Periods of Starvation

Takano, Sotaro; Pawlowska, Bogna J.; Gudelj, Ivana; Yomo, Tetsuya; Tsuru, Saburo

doi:10.1128/mbio.02336-16

Cited by 47 publications

(66 citation statements)

References 48 publications

(52 reference statements)

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“…The rpoS819 mediated GASP has been directly correlated with enhanced ability to scavenge amino acids, the key nutrients released by dead cells. This can be modulated by altering environmental factors such as pH of the medium (11,15,52). Strong selection for rpoS92, which partially recovers RpoS activity, indicates further tuning of RpoS activity.…”

Section: Discussionmentioning

confidence: 99%

“…E. coli survival during prolonged stationary-phase is illustrated by the phenomenon of Growth Advantage in Stationary-Phase (GASP). During GASP, genetic variants called GASP mutants arise and proliferate in the primarily non-growth environment of prolonged stationary-phase, presumably by extracting nutrients from dead cell debris (10)(11)(12)(13)(14)(15).…”

Section: Introductionmentioning

confidence: 99%

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Modulation ofrpoSfitness by loss ofcpdAactivity during stationary-phase inEscherichia coli

Chib

Seshasayee

2018

Preprint

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Experimental evolution of Escherichia coli in one month long stationary-phase in lysogeny broth batch cultures repeatedly selected mutations in the genes for the stationary-phase sigma factor RpoS and the cAMP phosphodiesterase CpdA. The founder strain carried a previously identified allele of rpoS, referred to as rpoS819, a partially functional variant that confers growth advantage in stationary-phase (GASP). The 46 base duplication at the 3' end of rpoS819 produces a longer protein present at very low levels compared to wild type RpoS. A new rpoS variant rpoS92, carrying a re-duplication of the original duplication in rpoS819, arose during the first week of our evolution experiment. In rpoS92, an in-frame stop codon truncated RpoS819 creating a shorter RpoS92 whose levels are restored to that of wild type RpoS. Transcription profiling of rpoS92 indicated a shift in gene-expression to that of wild-type rpoS, reversing some of the expression trends of rpoS819. Δ3cpdA, carrying an in-frame three base deletion, had arisen late in our evolution experiment. It is a loss of function mutation, which elevates cAMP levels. Using mixed culture competition experiments, we demonstrate that rpoS92 confers GASP, whereas Δ3cpdA confers relatively modest GASP in comparison to the ancestral rpoS819. Δ3cpdA mediates epistatic repression of rpoS92 GASP. The original survivor carrying both rpoS92 and Δ3cpdA besides other mutations displays robust GASP, highlighting the role of these additional mutations in reversing the epistatic interaction between Δ3cpdA and rpoS92. In 10-and 20-day old spent media, there is a reduction in the competitive fitness of rpoS92, which is arrested by Δ3cpdA. Thus the activity of RpoS fluctuates via genetic mutations in deep stationary phase, and additional mutations in CpdA helps modulate the competitive fitness of RpoS variants.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Modulation ofrpoSfitness by loss ofcpdAactivity during stationary-phase inEscherichia coli

Chib

Seshasayee

2018

Preprint

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“…But the exact same questions remain to be elucidated in this field: how many cell divisions happen in these starving colonies? In batch cultures, is stationary phase really stationary, or is there some turnover and recycling as recently suggested [48]? And more importantly, where does death come from: is it an unavoidable, externally caused phenomenon; or is there an internal component, such as an altruistic programmed cell death [50], or just traits selected in other environments that give a maladaptation to certain stresses [23]?…”

Section: Discussionmentioning

confidence: 99%

Death and population dynamics affect mutation rate estimates and evolvability under stress in bacteria

Frénoy

Bonhoeffer

2017

Preprint

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The stress-induced mutagenesis paradigm postulates that in response to stress, bacteria increase their genome-wide mutation rate, in turn increasing the chances that a descendant is able to withstand the stress. This has implications for antibiotic treatment: exposure to sub-inhibitory doses of antibiotics has been reported to increase bacterial mutation rates, and thus probably the rate at which resistance mutations appear and lead to treatment failure.Measuring mutation rates under stress, however, is problematic, because existing methods assume there is no death. Yet sub-inhibitory stress levels may induce a substantial death rate. Death events need to be compensated by extra replication to reach a given population size, thus giving more opportunities to acquire mutations. We show that ignoring death leads to a systematic overestimation of mutation rates under stress.We developed a system using plasmid segregation to measure death and growth rates simultaneously in bacterial populations. We use it to replicate classical experiments reporting antibioticinduced mutagenesis. We found that a substantial death rate occurs at the tested sub-inhibitory concentrations, and taking this death into account lowers and sometimes removes the signal for stress-induced mutagenesis. Moreover even when antibiotics increase mutation rate, sub-inhibitory treatments do not increase genetic diversity and evolvability, again because of effects of the antibiotics on population dynamics.Beside showing that population dynamic is a crucial but neglected parameter affecting evolvability, we provide better experimental and computational tools to study evolvability under stress, leading to a re-assessment of the magnitude and significance of the stress-induced mutagenesis paradigm.

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“…However, the study unfortunately failed to remove the dead cells in the long‐term stationary phase. A recent study showed that nutrients in the culture are supplied from the dead cells who exist in large numbers, and the bacterial growth was restricted by cell‐to‐cell interactions before the exhaustion of nutrients in such conditions (Takano et al, ). These new findings suggest unclearness or complexity of selective pressure in the long‐term stationary phase.…”

Section: Discussionmentioning

confidence: 99%

“…However, this evolution experiment consists of very complicated selections during extensive death phase and long‐term stationary phase. For instance, our recent study found that the resources are not limited in the long‐term stationary phase due to leakage from dead cells (Takano, Pawlowska, Gudelj, Yomo, & Tsuru, ), implying that selections act on the other traits rather than histidine utilization. Thus, it is still unknown whether the mutations improving carrying capacity in histidine utilization are pervasive or not.…”

Section: Introductionmentioning

confidence: 99%

Enhancement of K‐strategy evolution in histidine utilization using a container with compartments

et al. 2018

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Evolutionary strategies in growth improvement can be classified into r- or K-strategies. The former strategy corresponds to an evolutionary increase in growth rate, whereas the latter corresponds to an increase in the maximum amount of organisms or carrying capacity. What determines the strategies to be adopted during evolution? Spatial structures that compartmentalize the population into small patches are key to inducing the K-strategy. Interestingly, previous evolution experiments using Escherichia coli in a glucose-limited batch culture showed that carrying capacity could improve evolutionally even in the absence of spatial structures. However, it is unclear if the lack of spatial structures can direct evolution toward high carrying capacity for utilization of other resources. To address this question, we established a simplified evolution experiment using histidine-requiring E. coli grown under histidine limitation in a container with compartments. We confirmed the importance of spatial structures in K-strategy evolution in histidine utilization. Whole genome sequencing of the K-adapted strains showed functional variety of the mutated genes during the fitness-increasing period. These results validate the importance of spatial structures and imply that restriction of K-strategy evolution on a sort of nutrients is attributable to a paucity of appropriate selection rather than a paucity of causal mutation.

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Density-Dependent Recycling Promotes the Long-Term Survival of Bacterial Populations during Periods of Starvation

Cited by 47 publications

References 48 publications

Modulation ofrpoSfitness by loss ofcpdAactivity during stationary-phase inEscherichia coli

Modulation ofrpoSfitness by loss ofcpdAactivity during stationary-phase inEscherichia coli

Death and population dynamics affect mutation rate estimates and evolvability under stress in bacteria

Enhancement of K‐strategy evolution in histidine utilization using a container with compartments

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