Modelling bacterial chemotaxis for indirectly binding attractants

Tan, Pei Yen; Marcos, .; Liu, Yu

doi:10.1016/j.jtbi.2019.110120

Cited by 2 publications

(4 citation statements)

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“…As a result of our assumption of low periplasmic concentrations of maltose, we cannot make the common simplifying assumption that the free periplasmic chemoattractant concentration is independent of the abundance of chemoreceptors (19,35,37). We instead assume that the concentration of bound receptors is…”

Section: Resultsmentioning

confidence: 99%

“…Therefore, when maltose is present in micromolar concentrations in the environment, there are estimated to be significantly lower concentrations of free maltose within the periplasm (24,26,(30)(31)(32)(33)(34). Indeed, Tan and coworkers recently suggested that the periplasmic concentration of free maltose must be lower than the extracellular concentration, based on a discrepancy they found when fitting data of E. coli capillary assays to their population-level chemotaxis model, which accounted for indirect binding (35).…”

Section: Introductionmentioning

confidence: 99%

“…Our transport-and-sensing chemotaxis model incorporates the impact of variable porin and transporter expression on the chemotactic response. Importantly, due to the limiting concentrations of free maltose in the periplasm, our model removes the common simplifying assumption that the free periplasmic concentration of the sensed substrate is independent of the abundance of chemoreceptors (19,35,37) and instead explicitly considers how the chemotactic signal is a function of chemoreceptor abundance.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

Norris

Alcolombri

Keegstra

et al. 2022

Biophysical Journal

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

Norris

Alcolombri

Keegstra

et al. 2022

Biophysical Journal

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Section: Introductionmentioning

confidence: 99%

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

Norris

Alcolombri

et al. 2021

Preprint

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To swim up gradients of nutrients, E. coli senses nutrient concentrations within its periplasm. For small nutrient molecules, periplasmic concentrations typically match extracellular concentrations. However, this is not necessarily the case for saccharides, such as maltose, which is transported into the periplasm via a specific porin. Previous observations have shown that under various conditions E. coli limits maltoporin abundance so that, for extracellular micromolar concentrations of maltose, there are predicted to be only nanomolar concentrations of free maltose in the periplasm. Thus, in the micromolar regime, the total uptake of maltose from the external environment into the cytoplasm is limited not by the abundance of cytoplasmic transport proteins but by the abundance of maltoporins. Here we present results from experiments and modeling showing that this porin-limited transport enables E. coli to sense micromolar gradients of maltose despite having a high-affinity ABC transport system that is saturated at these micromolar levels. We used microfluidic assays to study chemotaxis of E. coli in various gradients of maltose and methyl-aspartate and leveraged our experimental observations to develop a mechanistic transport-and-sensing chemotaxis model. Incorporating this model into agent-based simulations, we discover a trade-off between uptake and sensing: although high-affinity transport enables higher uptake rates at low nutrient concentrations, it severely limits dynamic sensing range. We thus propose that E. coli may limit periplasmic uptake to increase its chemotactic sensitivity, enabling it to use maltose as an environmental cue.Statement of SignificanceBacterial chemotaxis is among the best-studied systems in biology and is paradigmatic of the mechanisms used by cells to link sensory inputs with regulated responses, thus providing insight into the ecological basis of cellular physiology. Here we present a mechanistic chemotaxis model that describes how the regulation of the transport of a sugar into and out of the cell’s periplasm affects the cell’s motile response to that sugar. Based on observations from population-level chemotaxis assays, we uncover an ecologically relevant trade-off between sensing and uptake. The general finding of this work is that, while high-affinity transport allows for higher uptake rates, it can severely limit the cell’s dynamic sensing range.

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Modelling bacterial chemotaxis for indirectly binding attractants

Cited by 2 publications

References 68 publications

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

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