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Subpopulations of sensorless bacteria drive fitness in fluctuating environments

Populations of bacteria often undergo a lag in growth when switching conditions. Because growth lags can be large compared to typical doubling times, variations in growth lag are an important but often overlooked component of bacterial fitness in fluctuating environments. We here explore how growth...

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Autores principales: Julou, Thomas, Zweifel, Ludovit, Blank, Diana, Fiori, Athos, van Nimwegen, Erik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7738171/
https://www.ncbi.nlm.nih.gov/pubmed/33270631
http://dx.doi.org/10.1371/journal.pbio.3000952
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author Julou, Thomas
Zweifel, Ludovit
Blank, Diana
Fiori, Athos
van Nimwegen, Erik
author_facet Julou, Thomas
Zweifel, Ludovit
Blank, Diana
Fiori, Athos
van Nimwegen, Erik
author_sort Julou, Thomas
collection PubMed
description Populations of bacteria often undergo a lag in growth when switching conditions. Because growth lags can be large compared to typical doubling times, variations in growth lag are an important but often overlooked component of bacterial fitness in fluctuating environments. We here explore how growth lag variation is determined for the archetypical switch from glucose to lactose as a carbon source in Escherichia coli. First, we show that single-cell lags are bimodally distributed and controlled by a single-molecule trigger. That is, gene expression noise causes the population before the switch to divide into subpopulations with zero and nonzero lac operon expression. While “sensorless” cells with zero preexisting lac expression at the switch have long lags because they are unable to sense the lactose signal, any nonzero lac operon expression suffices to ensure a short lag. Second, we show that the growth lag at the population level depends crucially on the fraction of sensorless cells and that this fraction in turn depends sensitively on the growth condition before the switch. Consequently, even small changes in basal expression can significantly affect the fraction of sensorless cells, thereby population lags and fitness under switching conditions, and may thus be subject to significant natural selection. Indeed, we show that condition-dependent population lags vary across wild E. coli isolates. Since many sensory genes are naturally low expressed in conditions where their inducer is not present, bimodal responses due to subpopulations of sensorless cells may be a general mechanism inducing phenotypic heterogeneity and controlling population lags in switching environments. This mechanism also illustrates how gene expression noise can turn even a simple sensory gene circuit into a bet hedging module and underlines the profound role of gene expression noise in regulatory responses.
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spelling pubmed-77381712020-12-28 Subpopulations of sensorless bacteria drive fitness in fluctuating environments Julou, Thomas Zweifel, Ludovit Blank, Diana Fiori, Athos van Nimwegen, Erik PLoS Biol Research Article Populations of bacteria often undergo a lag in growth when switching conditions. Because growth lags can be large compared to typical doubling times, variations in growth lag are an important but often overlooked component of bacterial fitness in fluctuating environments. We here explore how growth lag variation is determined for the archetypical switch from glucose to lactose as a carbon source in Escherichia coli. First, we show that single-cell lags are bimodally distributed and controlled by a single-molecule trigger. That is, gene expression noise causes the population before the switch to divide into subpopulations with zero and nonzero lac operon expression. While “sensorless” cells with zero preexisting lac expression at the switch have long lags because they are unable to sense the lactose signal, any nonzero lac operon expression suffices to ensure a short lag. Second, we show that the growth lag at the population level depends crucially on the fraction of sensorless cells and that this fraction in turn depends sensitively on the growth condition before the switch. Consequently, even small changes in basal expression can significantly affect the fraction of sensorless cells, thereby population lags and fitness under switching conditions, and may thus be subject to significant natural selection. Indeed, we show that condition-dependent population lags vary across wild E. coli isolates. Since many sensory genes are naturally low expressed in conditions where their inducer is not present, bimodal responses due to subpopulations of sensorless cells may be a general mechanism inducing phenotypic heterogeneity and controlling population lags in switching environments. This mechanism also illustrates how gene expression noise can turn even a simple sensory gene circuit into a bet hedging module and underlines the profound role of gene expression noise in regulatory responses. Public Library of Science 2020-12-03 /pmc/articles/PMC7738171/ /pubmed/33270631 http://dx.doi.org/10.1371/journal.pbio.3000952 Text en © 2020 Julou et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Julou, Thomas
Zweifel, Ludovit
Blank, Diana
Fiori, Athos
van Nimwegen, Erik
Subpopulations of sensorless bacteria drive fitness in fluctuating environments
title Subpopulations of sensorless bacteria drive fitness in fluctuating environments
title_full Subpopulations of sensorless bacteria drive fitness in fluctuating environments
title_fullStr Subpopulations of sensorless bacteria drive fitness in fluctuating environments
title_full_unstemmed Subpopulations of sensorless bacteria drive fitness in fluctuating environments
title_short Subpopulations of sensorless bacteria drive fitness in fluctuating environments
title_sort subpopulations of sensorless bacteria drive fitness in fluctuating environments
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7738171/
https://www.ncbi.nlm.nih.gov/pubmed/33270631
http://dx.doi.org/10.1371/journal.pbio.3000952
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