Tightly Regulated and Heritable Division Control in Single Bacterial Cells

Siegal-Gaskins, Dan; Crosson, Sean

doi:10.1529/biophysj.108.128785

Cited by 63 publications

(66 citation statements)

References 55 publications

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“…The limited available studies on individual cell behavioral noise focus on the division times of a single cell, with the daughter cells being removed (14)(15)(16). The distributions of these division times can be used to describe the growth of microbial populations through a birth model (30).…”

Section: Heterogeneity In the Colonial Growth Dynamics Of Single Cellsmentioning

confidence: 99%

Stochasticity in Colonial Growth Dynamics of Individual Bacterial Cells

Koutsoumanis

Nychas

2013

Appl Environ Microbiol

103

104

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Conventional bacterial growth studies rely on large bacterial populations without considering the individual cells. Individual cells, however, can exhibit marked behavioral heterogeneity. Here, we present experimental observations on the colonial growth of 220 individual cells of Salmonella enterica serotype Typhimurium using time-lapse microscopy videos. We found a highly heterogeneous behavior. Some cells did not grow, showing filamentation or lysis before division. Cells that were able to grow and form microcolonies showed highly diverse growth dynamics. The quality of the videos allowed for counting the cells over time and estimating the kinetic parameters lag time () and maximum specific growth rate ( max ) for each microcolony originating from a single cell. To interpret the observations, the variability of the kinetic parameters was characterized using appropriate probability distributions and introduced to a stochastic model that allows for taking into account heterogeneity using Monte Carlo simulation. The model provides stochastic growth curves demonstrating that growth of single cells or small microbial populations is a pool of events each one of which has its own probability to occur. Simulations of the model illustrated how the apparent variability in population growth gradually decreases with increasing initial population size (N 0 ). For bacterial populations with N 0 of >100 cells, the variability is almost eliminated and the system seems to behave deterministically, even though the underlying law is stochastic. We also used the model to demonstrate the effect of the presence and extent of a nongrowing population fraction on the stochastic growth of bacterial populations.All the physical and chemical laws that are known to play an important part in the life of organisms are of statistical kind.

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Section: Heterogeneity In the Colonial Growth Dynamics Of Single Cellsmentioning

confidence: 99%

Stochasticity in Colonial Growth Dynamics of Individual Bacterial Cells

Koutsoumanis

Nychas

2013

Appl Environ Microbiol

103

104

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“…For example, early observations of isolated cells under a light microscope demonstrated a unimodal distribution of fission times (Powell 1958). More recently, the development of microfluidic devices has allowed for detailed single-cell observations of bacterial fission on an unprecedented scale (Elfwing et al 2004;Wakamoto et al 2005;Siegal-Gaskins and Crosson 2008), demonstrating that fission times within the first few generations of a lineage remain correlated, with a CV of 30%.Finally, bacterial populations in batch culture have become perhaps the most influential model system for the study of adaptation (Kawecki et al 2012;Kussell 2012;Barrick and Lenski 2013), and growth in batch culture is characterized by its own "life-history" traits. In particular, growth begins only after a well-documented delay, the lag phase, and continues until the population density is high and resources are depleted; when resources are sufficiently low, cell replication ceases and the relatively quiescent stationary phase begins.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

Survival Probability of Beneficial Mutations in Bacterial Batch Culture

Wahl

Zhu²

2015

Genetics

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The survival of rare beneficial mutations can be extremely sensitive to the organism's life history and the trait affected by the mutation. Given the tremendous impact of bacteria in batch culture as a model system for the study of adaptation, it is important to understand the survival probability of beneficial mutations in these populations. Here we develop a life-history model for bacterial populations in batch culture and predict the survival of mutations that increase fitness through their effects on specific traits: lag time, fission time, viability, and the timing of stationary phase. We find that if beneficial mutations are present in the founding population at the beginning of culture growth, mutations that reduce the mortality of daughter cells are the most likely to survive drift. In contrast, of mutations that occur de novo during growth, those that delay the onset of stationary phase are the most likely to survive. Our model predicts that approximately fivefold population growth between bottlenecks will optimize the occurrence and survival of beneficial mutations of all four types. This prediction is relatively insensitive to other model parameters, such as the lag time, fission time, or mortality rate of the population. We further estimate that bottlenecks that are more severe than this optimal prediction substantially reduce the occurrence and survival of adaptive mutations.KEYWORDS fixation probability; serial passaging; adaptation; experimental evolution; life history I T is well understood that most de novo mutations, even if they confer a substantial fitness advantage to the organism, do not survive the vicissitudes of genetic drift when initially rare (Fisher 1922;Haldane 1927;Wright 1929;Kimura 1964). The influences of population size, population structure, and environmental fluctuations on the fate of beneficial mutations have all been well studied, including cyclic (Otto and Whitlock 1997;Pollak 2000) or dynamically changing population sizes (Lambert 2006; Parsons and Quince 2007a,b), population subdivision (Barton 1993;Cherry 2003;Whitlock 2003) and migration (Lundy and Possingham 1998;Shpak and Proulx 2007), fluctuating selection (Haccou and Iwasa 1996;Lande 2007), or several of these factors in combination (Uecker and Hermisson 2011;Waxman 2011).A phenomenon that is perhaps less well appreciated is the sensitivity of a beneficial mutation's fate-survival or extinction-to the details of the organism's life history and the trait affected by the mutation. Studies of the extinction process in a population of changing size have demonstrated that extinction probabilities sensitively depend on whether mutations increase birth rates or reduce death rates (Parsons and Quince 2007a,b) or if mutations affect other life-history traits (Lambert 2006). Previous work has also compared the fate of mutations that reduce generation times with those that increase offspring survival (Wahl and Dehaan 2004). From these studies a clear picture is emerging: beneficial mutations that confer the same ...

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“…12 This design has been adopted by a variety of microfluidic perfusion devices. 13,14 However, in this case, the high speed generates a high shear stress, which is generally harmful for cells. There still exist a number of problems when wanting higher performance, such as high sensitivity, good biocompatibility and fine microfluidic culture.…”

Section: Microfluidic Device Designmentioning

confidence: 99%

“…12 By implementing the design to mechanically decouple cells from the fluid, the aforementioned issues could be addressed successfully. 13,14 In this paper, a novel microfluidic structure is proposed to acquire a stable and isolated microenvironment. The Finite Element Method (FEM) is used to predict the fluid transport properties for a minimum fluid disturbance, based on a specific chamber structure.…”

Section: Introductionmentioning

confidence: 99%

A zero-flow microfluidics for long-term cell culture and detection

et al. 2014

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A zero-flow microfluidic design is proposed in this paper, which can be used for long-term cell culture and detection, especially for a lab-on-chip integrated with a biosensor. It consists of two parts: a main microchannel; and a circle microchamber. The Finite Element Method (FEM) was employed to predict the fluid transport properties for a minimum fluid flow disturbance. Some commonly used microfluidic structures were also analysed systematically to prove the designed structure. Then the designed microfluidics was fabricated. Based on the simulations and experiments, this design provides a continuous flow environment, with a relatively stable and low shear stress atmosphere, similar to a zero-flow environment. Furthermore, the nutrients maintaining cells’ normal growth can be taken into the chamber through the diffusion effect. It also proves that the microfluidics can realize long-term cell culture and detection. The application of the structure in the field of biological microelectromechenical systems (BioMEMS) will provide a research foundation for microfluidic technology.

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Tightly Regulated and Heritable Division Control in Single Bacterial Cells

Cited by 63 publications

References 55 publications

Stochasticity in Colonial Growth Dynamics of Individual Bacterial Cells

Stochasticity in Colonial Growth Dynamics of Individual Bacterial Cells

Survival Probability of Beneficial Mutations in Bacterial Batch Culture

A zero-flow microfluidics for long-term cell culture and detection

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