Escherichia coli swimming is robust against variations in flagellar number

Mears, Patrick J.; Koirala, Santosh; Rao, Chris V; Golding, Ido; Chemla, Yann R.

doi:10.7554/elife.01916

Cited by 78 publications

(110 citation statements)

References 44 publications

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“…The distribution of tumble biases was unimodal with mode at 0.2 and a standard deviation of 0.093 (Fig 1C). These values are consistent with the previously reported distribution of single flagellar motor biases from tethered cells [29] and taking into account the effect of multiple flagella that increases the cell tumble bias relative to the clockwise bias of single motors [34,35]. As expected, we observed very few cells with tumble biases outside the 0.1 to 0.4 range because the robust architecture of the chemotaxis pathway ensures that the population tumble bias is maintained within a functional range [7,36–40].…”

Section: Resultssupporting

confidence: 92%

Direct Correlation between Motile Behavior and Protein Abundance in Single Cells

et al. 2016

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Understanding how stochastic molecular fluctuations affect cell behavior requires the quantification of both behavior and protein numbers in the same cells. Here, we combine automated microscopy with in situ hydrogel polymerization to measure single-cell protein expression after tracking swimming behavior. We characterized the distribution of non-genetic phenotypic diversity in Escherichia coli motility, which affects single-cell exploration. By expressing fluorescently tagged chemotaxis proteins (CheR and CheB) at different levels, we quantitatively mapped motile phenotype (tumble bias) to protein numbers using thousands of single-cell measurements. Our results disagreed with established models until we incorporated the role of CheB in receptor deamidation and the slow fluctuations in receptor methylation. Beyond refining models, our central finding is that changes in numbers of CheR and CheB affect the population mean tumble bias and its variance independently. Therefore, it is possible to adjust the degree of phenotypic diversity of a population by adjusting the global level of expression of CheR and CheB while keeping their ratio constant, which, as shown in previous studies, confers functional robustness to the system. Since genetic control of protein expression is heritable, our results suggest that non-genetic diversity in motile behavior is selectable, supporting earlier hypotheses that such diversity confers a selective advantage.

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Section: Resultssupporting

confidence: 92%

Direct Correlation between Motile Behavior and Protein Abundance in Single Cells

et al. 2016

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“…The rotating body in the first case or the rotating bead in the second is monitored as a function of time to determine the performance of the motor. More recently, the motor speed has been determined by trapping a cell with a laser tweezer and visualizing the fluorescently tagged flagella with the help of a high-speed camera (Mears et al 2014). Since all the aforementioned techniques apply to single cells, it is difficult to determine motor performance for a population of cells using such techniques due to the lack of a statistically significant number of cells tested (Eisenbach et al 1990).…”

Section: Introductionmentioning

confidence: 99%

Escherichia coli modulates its motor speed on sensing an attractant

et al. 2016

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It is well known that Escherichia coli achieves chemotaxis by modulating the bias of the flagellar motor. Recent experiments have shown that the bacteria vary their swimming speeds as well in presence of attractants. However, this increase in the swimming speed in response to the attractants has not been correlated with the increase in the flagellar motor speed. Using flickering dark-field microscopy, we measure the head-rotation speed of a large population of cells to correlate it with the flagellar motor speed. Experiments performed with wild-type and trg-deletion mutant strains suggest that the cells are capable of modulating the flagellar motor speed via mere sensing of a ligand. The motor speed can be further correlated with the swimming speed of the cells and was found to be linear. These results suggest the existence of a hitherto unknown intra-cellular pathway that modulates the flagellar motor speed in response to sensing of chemicals, thereby making chemotaxis more efficient than previously known.

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“…In fact, coupling between motors rotating in the CW direction, e.g. through their flagella, results in a tumble bias, which is robust against the number of motors, a design principle previously missed [7,[61][62][63].…”

Section: Cell-to-cell Variability and Cell Behaviormentioning

confidence: 99%

“…This technique helped to better understand the large variation in number of motors in E. coli [61]. In fact, coupling between motors rotating in the CW direction, e.g.…”

Section: Cell-to-cell Variability and Cell Behaviormentioning

confidence: 99%

Bacterial chemotaxis: information processing, thermodynamics, and behavior

Micali

Endres

2016

Current Opinion in Microbiology

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Escherichia coli has long been used as a model organism due to the extensive experimental characterization of its pathways and molecular components. Take chemotaxis as an example, which allows bacteria to sense and swim in response to chemicals, such as nutrients and toxins. Many of the pathway's remarkable sensing and signaling properties are now concisely summarized in terms of design (or engineering) principles. More recently, new approaches from information theory and stochastic thermodynamics have begun to address how pathways process environmental stimuli and what the limiting factors are. However, to fully capitalize on these theoretical advances, a closer connection with single-cell experiments will be required. IntroductionAll living organisms from animals to unicellular bacteria live under constant evolutionary pressure. To stay ahead in the game of evolution, organisms need to process noisy information, allowing them to make survival decisions quickly. However, to process information and move organisms also require energy. Thus the final behavior of any organism has to be an outcome which produces strong advantages under likely occurring environments. Chemotaxis of Escherichia coli is particularly well understood in terms of its molecular components, allowing this bacterium to migrate towards food and away from toxins [1][2][3][4][5]. Indeed, an ever increasing amount of studies has highlighted several design principles, i.e. engineering blue prints, ensuring exquisite sensitivity, efficiency, robustness, and wide dynamic range at all levels of the pathway.This review focuses on recent findings in E. coli chemotaxis, in particular on how molecular mechanisms give rise to information processing, its associated thermodynamic cost, and the resulting swimming behavior. What new design principles will be discovered next? Classical view of Escherichia coli chemotaxisEscherichia coli is a Gram-negative bacterium inhabiting soil, as well as the animal and human gastrointestinal tracts. Inside the host, it contributes to the digestion of food and enhances resistance against pathogens [6]. This bacterium has a relatively simple chemotactic pathway (Fig. 1 1A). External stimuli are processed at the receptor level, where receptors sense and memorize chemical concentrations from the past by their adapted methylation level (Fig. 1A, see red box for 'sensing module'). The receptor-signaling activity can be monitored experimentally by tagging the CheY and CheZ proteins with a fluorescence-resonance-energy-transfer (FRET) reporter pair to follow their phosphorylation-dependent interaction. To swim cells are equipped with 5-8 flagellar rotary motors (Fig. 1A, blue box for 'motility module'), each of which rotates either clockwise (CW) or counterclockwise (CCW). Taking together these flagella determine cell movement, given either by a 'run' or a random reorientation in a 'tumble' [7][8][9]. The phosphorylated protein CheY-p links sensing and motility (Fig. 1A). In absence of any chemical gradient E. coli per...

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Escherichia coli swimming is robust against variations in flagellar number

Cited by 78 publications

References 44 publications

Direct Correlation between Motile Behavior and Protein Abundance in Single Cells

Direct Correlation between Motile Behavior and Protein Abundance in Single Cells

Escherichia coli modulates its motor speed on sensing an attractant

Bacterial chemotaxis: information processing, thermodynamics, and behavior

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