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

Noele Norris*, Uria Alcolombri, Johannes M. Keegstra, Yutaka Yawata, Filippo Menolascina, Emilio Frazzoli, Naomi M. Levine, Vicente I. Fernandez, Roman Stocker*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

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 are 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 suggesting 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 the range of dynamic sensing. We thus propose that E. coli may limit periplasmic uptake to increase its chemotactic sensitivity, enabling it to use maltose as an environmental cue.

Original languageEnglish
Pages (from-to)2046-2059
Number of pages14
JournalBiophysical Journal
Volume121
Issue number11
DOIs
StatePublished - 7 Jun 2022
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2022

Keywords

  • ABC transport
  • bacterial chemotaxis
  • molecular-level model
  • population-level motility assay
  • porin-limited transport

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