Networked Chemoreceptors Benefit Bacterial Chemotaxis Performance

Frank, Vered; Piñas, Germán E.; Cohen, Harel; Parkinson, John S.; Vaknin, Ady

doi:10.1128/mbio.01824-16

Cited by 39 publications

(57 citation statements)

References 54 publications

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“…Results from "Imposed" simulations supported previous findings indicating that the ECP behavior is governed by receptor sensitivity rather than absolute attractant concentration [28,54]. Similarly, more recent biochemical work [55] has also substantiated the long-held notion that the networked architecture of chemosensory receptor arrays in E. coli plays a vital role in the cell's robust response behavior. Results of simulations that incorporate CLB-ADT emphasize the importance of advective-diffusive transport phenomena in modeling ECP trajectories in fluidic environments.…”

Section: Discussionsupporting

confidence: 73%

Effects of Advective-Diffusive Transport of Multiple Chemoattractants on Motility of Engineered Chemosensory Particles in Fluidic Environments

King

Başağaoğlu

Nguyen

et al. 2019

Entropy

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Motility behavior of an engineered chemosensory particle (ECP) in fluidic environments is driven by its responses to chemical stimuli. One of the challenges to understanding such behaviors lies in tracking changes in chemical signal gradients of chemoattractants and ECP-fluid dynamics as the fluid is continuously disturbed by ECP motion. To address this challenge, we introduce a new multiscale numerical model to simulate chemotactic swimming of an ECP in confined fluidic environments by accounting for motility-induced disturbances in spatiotemporal chemoattractant distributions. The model accommodates advective-diffusive transport of unmixed chemoattractants, ECP-fluid hydrodynamics at the ECP-fluid interface, and spatiotemporal disturbances in the chemoattractant concentrations due to particle motion. Demonstrative simulations are presented with an ECP, mimicking Escherichia coli (E. coli) chemotaxis, released into initially quiescent fluids with different source configurations of the chemoattractants N-methyl-L-aspartate and L-serine. Simulations demonstrate that initial distributions and temporal evolution of chemoattractants and their release modes (instantaneous vs. continuous, point source vs. distributed) dictate time histories of chemotactic motility of an ECP. Chemotactic motility is shown to be largely determined by spatiotemporal variation in chemoattractant concentration gradients due to transient disturbances imposed by ECP-fluid hydrodynamics, an observation not captured in previous numerical studies that relied on static chemoattractant concentration fields.

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Section: Discussionsupporting

confidence: 73%

Effects of Advective-Diffusive Transport of Multiple Chemoattractants on Motility of Engineered Chemosensory Particles in Fluidic Environments

King

Başağaoğlu

Nguyen

et al. 2019

Entropy

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“…In fact, it has been previously shown that a strain, where FrzCD molecules can no longer bind DNA and are, thus, diffused (Figure 1) can still produce reversals (Bustamante et al, 2004). In E. coli chemosensory cluster formation is also not critical for signal transduction but it confers properties such as the amplification of signal, a direct consequence of the cooperative interactions between clustered chemoreceptors [11–15]. Thus, we decided to check if the formation of DNA-bound Frz clusters can also promote cooperativity in the signaling activity of the Frz chemosensory system.…”

Section: Resultsmentioning

confidence: 99%

“…Receptor clustering is not strictly required for signal transduction, as one functional unit is enough to generate phosphorylated CheY [6,9–11]. However, MCP clustering is essential to ensure the amplification of the initial signal, which is a direct consequence of the cooperative interactions between clustered chemoreceptors [11–15].…”

Section: Introductionmentioning

confidence: 99%

The nucleoid as a scaffold for the assembly of bacterial signaling complexes

Moine

Espinosa

Martineau

et al. 2017

Preprint

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The FrzCD chemoreceptor from the gliding bacterium Myxococcus xanthus forms cytoplasmic clusters that occupy a large central region of the cell body also occupied by the nucleoid. In this work, we show that FrzCD directly binds to the nucleoid with its N-terminal positively charged tail and recruits active signaling complexes at this location. The FrzCD binding to the nucleoid occur in a DNA-sequence independent manner and leads to the formation of multiple distributed clusters that explore constrained areas. This organization might be required for cooperative interactions between clustered receptors as observed in membrane-bound chemosensory arrays.AUTHOR SUMMARYIn this work, we show that the cytoplasmic chemoreceptor of the Frz chemosensory system, FrzCD, does not bind the cytoplasmic membrane like most MCPs but bind the bacterial nucleoid directly, thus forming distributed protein clusters also containing the Frz kinase. In vitro and in vivo experiments show that DNA-binding is not sequence-specific and is mediated by a basic aminoacid sequence of the FrzCD N-terminal domain. The deletion of this motif abolishes FrzCD DNA-binding and cooperativity in the response to signals. This work shows the importance of the nucleoid in the organization and functioning of cytoplasmic signaling systems in bacteria.

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“…The networking of signaling complexes in extended arrays leads to a cooperative response with enhanced sensitivity and dynamic range (20, 32, 39, 40), ultimately resulting in robust chemotactic performance (41). However, our understanding of how receptors collaboratively control kinase activity within an array is limited.…”

Section: Figmentioning

confidence: 99%

New Twists and Turns in Bacterial Locomotion and Signal Transduction

et al. 2019

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Prokaryotic organisms occupy the most diverse set of environments and conditions on our planet. Their ability to sense and respond to a broad range of external cues remain key research areas in modern microbiology, central to behaviors that underlie beneficial and pathogenic interactions of bacteria with multicellular organisms and within complex ecosystems. Advances in our understanding of the one- and two-component signal transduction systems that underlie these sensing pathways have been driven by advances in imaging the behavior of many individual bacterial cells, as well as visualizing individual proteins and protein arrays within living cells. Cryo-electron tomography continues to provide new insights into the structure and function of chemosensory receptors and flagellar motors, while advances in protein labeling and tracking are applied to understand information flow between receptor and motor. Sophisticated microfluidics allow simultaneous analysis of the behavior of thousands of individual cells, increasing our understanding of how variance between individuals is generated, regulated, and employed to maximize fitness of a population. In vitro experiments have been complemented by the study of signal transduction and motility in complex in vivo models, allowing investigators to directly address the contribution of motility, chemotaxis, and aggregation/adhesion on virulence during infection. Finally, systems biology approaches have demonstrated previously uncharted areas of protein space in which novel two-component signal transduction pathways can be designed and constructed de novo. These exciting experimental advances were just some of the many novel findings presented at the 15th Bacterial Locomotion and Signal Transduction conference (BLAST XV) in January 2019.

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Networked Chemoreceptors Benefit Bacterial Chemotaxis Performance

Cited by 39 publications

References 54 publications

Effects of Advective-Diffusive Transport of Multiple Chemoattractants on Motility of Engineered Chemosensory Particles in Fluidic Environments

Effects of Advective-Diffusive Transport of Multiple Chemoattractants on Motility of Engineered Chemosensory Particles in Fluidic Environments

The nucleoid as a scaffold for the assembly of bacterial signaling complexes

New Twists and Turns in Bacterial Locomotion and Signal Transduction

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