Literature DB >> 35526093

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

Noele Norris1, Uria Alcolombri2, Johannes M Keegstra2, Yutaka Yawata3, Filippo Menolascina4, Emilio Frazzoli5, Naomi M Levine6, Vicente I Fernandez2, Roman Stocker7.   

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. Published by Elsevier Inc.

Entities:  

Keywords:  ABC transport; bacterial chemotaxis; molecular-level model; population-level motility assay; porin-limited transport

Mesh:

Substances:

Year:  2022        PMID: 35526093      PMCID: PMC9247477          DOI: 10.1016/j.bpj.2022.05.003

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   3.699


  58 in total

1.  Role of the receptor for bacteriophage lambda in the functioning of the maltose chemoreceptor of Escherichia coli.

Authors:  G L Hazelbauer
Journal:  J Bacteriol       Date:  1975-10       Impact factor: 3.490

Review 2.  Learning new tricks from an old dog: MalT of the Escherichia coli maltose system is part of a complex regulatory network.

Authors:  W Boos; A Böhm
Journal:  Trends Genet       Date:  2000-09       Impact factor: 11.639

Review 3.  Microbial physiology and ecology of slow growth.

Authors:  A L Koch
Journal:  Microbiol Mol Biol Rev       Date:  1997-09       Impact factor: 11.056

4.  Mutations that alter the transport function of the LamB protein in Escherichia coli.

Authors:  C Wandersman; M Schwartz
Journal:  J Bacteriol       Date:  1982-07       Impact factor: 3.490

5.  Response rescaling in bacterial chemotaxis.

Authors:  Milena D Lazova; Tanvir Ahmed; Domenico Bellomo; Roman Stocker; Thomas S Shimizu
Journal:  Proc Natl Acad Sci U S A       Date:  2011-08-01       Impact factor: 11.205

6.  Quantitative modeling of Escherichia coli chemotactic motion in environments varying in space and time.

Authors:  Lili Jiang; Qi Ouyang; Yuhai Tu
Journal:  PLoS Comput Biol       Date:  2010-04-08       Impact factor: 4.475

7.  Opposite responses by different chemoreceptors set a tunable preference point in Escherichia coli pH taxis.

Authors:  Yiling Yang; Victor Sourjik
Journal:  Mol Microbiol       Date:  2012-11-05       Impact factor: 3.501

8.  Facilitated diffusion of p-nitrophenyl-alpha-D-maltohexaoside through the outer membrane of Escherichia coli. Characterization of LamB as a specific and saturable channel for maltooligosaccharides.

Authors:  S Freundlieb; U Ehmann; W Boos
Journal:  J Biol Chem       Date:  1988-01-05       Impact factor: 5.157

9.  A direct-sensing galactose chemoreceptor recently evolved in invasive strains of Campylobacter jejuni.

Authors:  Christopher J Day; Rebecca M King; Lucy K Shewell; Greg Tram; Tahria Najnin; Lauren E Hartley-Tassell; Jennifer C Wilson; Aaron D Fleetwood; Igor B Zhulin; Victoria Korolik
Journal:  Nat Commun       Date:  2016-10-20       Impact factor: 14.919

10.  Evaluation of the rate constants of sugar transport through maltoporin (LamB) of Escherichia coli from the sugar-induced current noise.

Authors:  C Andersen; M Jordy; R Benz
Journal:  J Gen Physiol       Date:  1995-03       Impact factor: 4.086

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