Need‐based activation of ammonium uptake in Escherichia coli

Abstract The efficient sequestration of nutrients is vital for the growth and survival of microorganisms. Some nutrients, such as CO2 and NH3, are readily diffusible across the cell membrane. The large membrane permeability of these nutrients obviates the need of transporters when the ambient level...

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Main Authors: Minsu Kim, Zhongge Zhang, Hiroyuki Okano, Dalai Yan, Alexander Groisman, Terence Hwa
Format: Article
Language:English
Published: Springer Nature 2012-09-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.1038/msb.2012.46
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author Minsu Kim
Zhongge Zhang
Hiroyuki Okano
Dalai Yan
Alexander Groisman
Terence Hwa
author_facet Minsu Kim
Zhongge Zhang
Hiroyuki Okano
Dalai Yan
Alexander Groisman
Terence Hwa
author_sort Minsu Kim
collection DOAJ
description Abstract The efficient sequestration of nutrients is vital for the growth and survival of microorganisms. Some nutrients, such as CO2 and NH3, are readily diffusible across the cell membrane. The large membrane permeability of these nutrients obviates the need of transporters when the ambient level is high. When the ambient level is low, however, maintaining a high intracellular nutrient level against passive back diffusion is both challenging and costly. Here, we study the delicate management of ammonium (NH4+/NH3) sequestration by E. coli cells using microfluidic chemostats. We find that as the ambient ammonium concentration is reduced, E. coli cells first maximize their ability to assimilate the gaseous NH3 diffusing into the cytoplasm and then abruptly activate ammonium transport. The onset of transport varies under different growth conditions, but always occurring just as needed to maintain growth. Quantitative modeling of known interactions reveals an integral feedback mechanism by which this need‐based uptake strategy is implemented. This novel strategy ensures that the expensive cost of upholding the internal ammonium concentration against back diffusion is kept at a minimum.
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institution Kabale University
issn 1744-4292
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publisher Springer Nature
record_format Article
series Molecular Systems Biology
spelling doaj-art-2b012ad1639e44fe83508ae581fb712b2025-08-20T03:46:37ZengSpringer NatureMolecular Systems Biology1744-42922012-09-018111010.1038/msb.2012.46Need‐based activation of ammonium uptake in Escherichia coliMinsu Kim0Zhongge Zhang1Hiroyuki Okano2Dalai Yan3Alexander Groisman4Terence Hwa5Department of Physics, University of California at San DiegoSection of Molecular Biology, Division of Biological Sciences, University of California at San DiegoDepartment of Physics, University of California at San DiegoDepartment of Microbiology and Immunology, Indiana University School of MedicineDepartment of Physics, University of California at San DiegoDepartment of Physics, University of California at San DiegoAbstract The efficient sequestration of nutrients is vital for the growth and survival of microorganisms. Some nutrients, such as CO2 and NH3, are readily diffusible across the cell membrane. The large membrane permeability of these nutrients obviates the need of transporters when the ambient level is high. When the ambient level is low, however, maintaining a high intracellular nutrient level against passive back diffusion is both challenging and costly. Here, we study the delicate management of ammonium (NH4+/NH3) sequestration by E. coli cells using microfluidic chemostats. We find that as the ambient ammonium concentration is reduced, E. coli cells first maximize their ability to assimilate the gaseous NH3 diffusing into the cytoplasm and then abruptly activate ammonium transport. The onset of transport varies under different growth conditions, but always occurring just as needed to maintain growth. Quantitative modeling of known interactions reveals an integral feedback mechanism by which this need‐based uptake strategy is implemented. This novel strategy ensures that the expensive cost of upholding the internal ammonium concentration against back diffusion is kept at a minimum.https://doi.org/10.1038/msb.2012.46active transportfutile cycleintegral feedbackmetabolic coordinationmicrofluidics
spellingShingle Minsu Kim
Zhongge Zhang
Hiroyuki Okano
Dalai Yan
Alexander Groisman
Terence Hwa
Need‐based activation of ammonium uptake in Escherichia coli
Molecular Systems Biology
active transport
futile cycle
integral feedback
metabolic coordination
microfluidics
title Need‐based activation of ammonium uptake in Escherichia coli
title_full Need‐based activation of ammonium uptake in Escherichia coli
title_fullStr Need‐based activation of ammonium uptake in Escherichia coli
title_full_unstemmed Need‐based activation of ammonium uptake in Escherichia coli
title_short Need‐based activation of ammonium uptake in Escherichia coli
title_sort need based activation of ammonium uptake in escherichia coli
topic active transport
futile cycle
integral feedback
metabolic coordination
microfluidics
url https://doi.org/10.1038/msb.2012.46
work_keys_str_mv AT minsukim needbasedactivationofammoniumuptakeinescherichiacoli
AT zhonggezhang needbasedactivationofammoniumuptakeinescherichiacoli
AT hiroyukiokano needbasedactivationofammoniumuptakeinescherichiacoli
AT dalaiyan needbasedactivationofammoniumuptakeinescherichiacoli
AT alexandergroisman needbasedactivationofammoniumuptakeinescherichiacoli
AT terencehwa needbasedactivationofammoniumuptakeinescherichiacoli