Cell size regulation in bacteria

Amir, Ariel

doi:10.1101/004457

Cited by 157 publications

(374 citation statements)

References 26 publications

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“…Indeed, cell size at birth and generation time are weakly correlated negatively (Pearson correlation coefficient, −0.48 ∼ −0.22; SI Appendix, Fig. S12), and this effect must be considered to account for cell size stability (3,(31)(32)(33)(34)(35). Nevertheless, our results suggest that, as far as age-related parameters and population growth rates are concerned, cell size information does not play a predominant role in E. coli over a broad set of culture conditions.…”

Section: Discussionmentioning

confidence: 48%

Noise-driven growth rate gain in clonal cellular populations

Hashimoto

Nozoe

Nakaoka

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

167

205

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Cellular populations in both nature and the laboratory are composed of phenotypically heterogeneous individuals that compete with each other resulting in complex population dynamics. Predicting population growth characteristics based on knowledge of heterogeneous single-cell dynamics remains challenging. By observing groups of cells for hundreds of generations at single-cell resolution, we reveal that growth noise causes clonal populations of Escherichia coli to double faster than the mean doubling time of their constituent single cells across a broad set of balanced-growth conditions. We show that the population-level growth rate gain as well as age structures of populations and of cell lineages in competition are predictable. Furthermore, we theoretically reveal that the growth rate gain can be linked with the relative entropy of lineage generation time distributions. Unexpectedly, we find an empirical linear relation between the means and the variances of generation times across conditions, which provides a general constraint on maximal growth rates. Together, these results demonstrate a fundamental benefit of noise for population growth, and identify a growth law that sets a "speed limit" for proliferation.growth noise | age-structured population model | cell lineage analysis | growth law | microfluidics C ell growth is an important physiological process that underlies the fitness of organisms. In exponentially growing cell populations, proliferation is usually quantified using the bulk population growth rate, which is assumed to represent the average growth rate of single cells within a population. In addition, basic growth laws exist that relate ribosome function and metabolic efficiency, macromolecular composition, and cell size of the culture as a whole to the bulk population growth rate (1-3). Population growth rate is therefore a quantity of primary importance that reports cellular physiological states and fitness.However, at the single-cell level, growth-related parameters such as the division time interval and division cell size are heterogeneous even in a clonal population growing at a constant rate (4-9). Such "growth noise" causes concurrently living cells to compete within the population for representation among its future descendants. For example, if two sibling cells born from the same mother cell had different division intervals, the faster dividing sibling is likely to have more descendants in the future population compared with its slower dividing sister, despite the fact that progenies of both siblings may proliferate equally well (Fig. 1). Intrapopulation competition complicates single-cell analysis because any growth-correlated quantities measured over the population deviate from intrinsic single-cell properties (10-12). In the case of the toy model described in Fig. 1, cells are assumed to determine their generation times (division interval) randomly by roll of a dice. The mean of intrinsic cellular generation time is thus ð1 + 2 + ⋯ + 6Þ=6 = 3.5 h, but population doubling time, which is...

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Section: Discussionmentioning

confidence: 48%

Noise-driven growth rate gain in clonal cellular populations

Hashimoto

Nozoe

Nakaoka

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

167

205

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“…A complete theory of bacterial cell shape should also account for the magnitudes of both radius and length; the regulation of these two is, however, of very different nature: Amir (2014) suggests a robust mechanism of maintaining cell length in bacteria, consistent with the experimentally observed correlations and distributions (Osella et al 2014;Robert et al 2014), invoking a simple biophysical mechanism that does not couple to mechanics or curvature. This mechanism is obviously decoupled from that of radius maintenance, as is proven by the possibility of having extremely long filamentuous cells which nevertheless maintain their constant radius (Amir et al 2013).…”

Section: Future Prospectsmentioning

confidence: 87%

Getting into shape: How do rod-like bacteria control their geometry?

Amir¹,

Teeffelen²

2014

Syst Synth Biol

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Rod-like bacteria maintain their cylindrical shapes with remarkable precision during growth. However, they are also capable to adapt their shapes to external forces and constraints, for example by growing into narrow or curved confinements. Despite being one of the simplest morphologies, we are still far from a full understanding of how shape is robustly regulated, and how bacteria obtain their near-perfect cylindrical shapes with excellent precision. However, recent experimental and theoretical findings suggest that cell-wall geometry and mechanical stress play important roles in regulating cell shape in rod-like bacteria. We review our current understanding of the cell wall architecture and the growth dynamics, and discuss possible candidates for regulatory cues of shape regulation in the absence or presence of external constraints. Finally, we suggest further future experimental and theoretical directions which may help to shed light on this fundamental problem.

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“…The expression f = 0 gives division size = V d = constant + noise, which corresponds to the critical size mode; f = 1 gives size increment = V d − V b = constant + noise, which corresponds to the critical increment mode; and f = 2 gives interdivision time = μ T × log 2 (V d /V b ) (given that cells grow at a constant relative rate) = μ T × log 2 (2 + μ b /V b × Z) ≈ constant + noise, which corresponds to specific time mode (4,37). The finding that cell volume grows at a constant relative rate implies that cell volume increases exponentially with time, so V(t) = V b e g t where, necessarily, g = ln2/μ T because, in homeostatic environments, cells double their volume, on average, over a cell cycle.…”

Section: Resultsmentioning

confidence: 99%

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Willis

Refahi

Wightman

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

185

217

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Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3-4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical size. Our data also rule out models in which cells undergo G2/M at a fixed time after birth, or by adding a critical size increment between G2/M transitions. Rather, cell size regulation was intermediate between the critical size and critical increment paradigms, meaning that cell size fluctuations decay by ∼75% in one generation compared with 100% (critical size) and 50% (critical increment). Notably, this behavior was independent of local cell-cell contact topologies and of position within the tissue. Cells grew exponentially throughout the first >80% of the cell cycle, but following an asymmetrical division, the small daughter grew at a faster exponential rate than the large daughter, an observation that potentially challenges present models of growth regulation. These growth and division behaviors place strong constraints on quantitative mechanistic descriptions of the cell cycle and growth control.cell size | cell growth | cell cycle | homeostasis | plant stem cells H ow cells coordinate growth and division to achieve a particular cell size remains a fundamental question in biology. Our understanding of this basic property of cells is limited, in part, by the lack of quantitative data on cellular growth and size kinetics over multiple generations, especially in higher eukaryotes (1). Classical studies of cell size homeostasis focused on whether division occurred upon reaching a critical size or after a fixed time period has elapsed (2, 3). However, time-lapse studies of single-celled organisms spanning a range of bacteria (4-7) and the yeast Saccharomyces cerevisiae (8) have recently indicated that cell size is regulated by the addition of a fixed volume increment between divisions. Identification of the size regulation behavior constrains the set of feasible molecular scenarios for how growth and division are coordinated with the cell cycle (8-10). In multicellular tissues, the loss of growth and division/cell cycle coordination could have an impact on the organism's development, yet, to the best of our knowledge, cell growth and size kinetics have never before been measured over generations in a tissue context. The experimental challenges are particularly acute because interdivision times are often on the order of tens of hours, cells have a diversity of shapes necessitating di...

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Cell size regulation in bacteria

Cited by 157 publications

References 26 publications

Noise-driven growth rate gain in clonal cellular populations

Noise-driven growth rate gain in clonal cellular populations

Getting into shape: How do rod-like bacteria control their geometry?

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

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