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Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli

Curli amyloid fibers are a major constituent of the extracellular biofilm matrix formed by bacteria of the Enterobacteriaceae family. Within Escherichia coli biofilms, curli gene expression is limited to a subpopulation of bacteria, leading to heterogeneity of extracellular matrix synthesis. Here we...

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Autores principales: Lamprecht, Olga, Ratnikava, Maryia, Jacek, Paulina, Kaganovitch, Eugen, Buettner, Nina, Fritz, Kirstin, Biazruchka, Ina, Köhler, Robin, Pietsch, Julian, Sourjik, Victor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212085/
https://www.ncbi.nlm.nih.gov/pubmed/37186613
http://dx.doi.org/10.1371/journal.pgen.1010750
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author Lamprecht, Olga
Ratnikava, Maryia
Jacek, Paulina
Kaganovitch, Eugen
Buettner, Nina
Fritz, Kirstin
Biazruchka, Ina
Köhler, Robin
Pietsch, Julian
Sourjik, Victor
author_facet Lamprecht, Olga
Ratnikava, Maryia
Jacek, Paulina
Kaganovitch, Eugen
Buettner, Nina
Fritz, Kirstin
Biazruchka, Ina
Köhler, Robin
Pietsch, Julian
Sourjik, Victor
author_sort Lamprecht, Olga
collection PubMed
description Curli amyloid fibers are a major constituent of the extracellular biofilm matrix formed by bacteria of the Enterobacteriaceae family. Within Escherichia coli biofilms, curli gene expression is limited to a subpopulation of bacteria, leading to heterogeneity of extracellular matrix synthesis. Here we show that bimodal activation of curli gene expression also occurs in well-mixed planktonic cultures of E. coli, resulting in all-or-none stochastic differentiation into distinct subpopulations of curli-positive and curli-negative cells at the entry into the stationary phase of growth. Stochastic curli activation in individual E. coli cells could further be observed during continuous growth in a conditioned medium in a microfluidic device, which further revealed that the curli-positive state is only metastable. In agreement with previous reports, regulation of curli gene expression by the second messenger c-di-GMP via two pairs of diguanylate cyclase and phosphodiesterase enzymes, DgcE/PdeH and DgcM/PdeR, modulates the fraction of curli-positive cells. Unexpectedly, removal of this regulatory network does not abolish the bimodality of curli gene expression, although it affects dynamics of activation and increases heterogeneity of expression levels among individual cells. Moreover, the fraction of curli-positive cells within an E. coli population shows stronger dependence on growth conditions in the absence of regulation by DgcE/PdeH and DgcM/PdeR pairs. We thus conclude that, while not required for the emergence of bimodal curli gene expression in E. coli, this c-di-GMP regulatory network attenuates the frequency and dynamics of gene activation and increases its robustness to cellular heterogeneity and environmental variation.
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spelling pubmed-102120852023-05-26 Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli Lamprecht, Olga Ratnikava, Maryia Jacek, Paulina Kaganovitch, Eugen Buettner, Nina Fritz, Kirstin Biazruchka, Ina Köhler, Robin Pietsch, Julian Sourjik, Victor PLoS Genet Research Article Curli amyloid fibers are a major constituent of the extracellular biofilm matrix formed by bacteria of the Enterobacteriaceae family. Within Escherichia coli biofilms, curli gene expression is limited to a subpopulation of bacteria, leading to heterogeneity of extracellular matrix synthesis. Here we show that bimodal activation of curli gene expression also occurs in well-mixed planktonic cultures of E. coli, resulting in all-or-none stochastic differentiation into distinct subpopulations of curli-positive and curli-negative cells at the entry into the stationary phase of growth. Stochastic curli activation in individual E. coli cells could further be observed during continuous growth in a conditioned medium in a microfluidic device, which further revealed that the curli-positive state is only metastable. In agreement with previous reports, regulation of curli gene expression by the second messenger c-di-GMP via two pairs of diguanylate cyclase and phosphodiesterase enzymes, DgcE/PdeH and DgcM/PdeR, modulates the fraction of curli-positive cells. Unexpectedly, removal of this regulatory network does not abolish the bimodality of curli gene expression, although it affects dynamics of activation and increases heterogeneity of expression levels among individual cells. Moreover, the fraction of curli-positive cells within an E. coli population shows stronger dependence on growth conditions in the absence of regulation by DgcE/PdeH and DgcM/PdeR pairs. We thus conclude that, while not required for the emergence of bimodal curli gene expression in E. coli, this c-di-GMP regulatory network attenuates the frequency and dynamics of gene activation and increases its robustness to cellular heterogeneity and environmental variation. Public Library of Science 2023-05-15 /pmc/articles/PMC10212085/ /pubmed/37186613 http://dx.doi.org/10.1371/journal.pgen.1010750 Text en © 2023 Lamprecht et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Lamprecht, Olga
Ratnikava, Maryia
Jacek, Paulina
Kaganovitch, Eugen
Buettner, Nina
Fritz, Kirstin
Biazruchka, Ina
Köhler, Robin
Pietsch, Julian
Sourjik, Victor
Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli
title Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli
title_full Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli
title_fullStr Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli
title_full_unstemmed Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli
title_short Regulation by cyclic di-GMP attenuates dynamics and enhances robustness of bimodal curli gene activation in Escherichia coli
title_sort regulation by cyclic di-gmp attenuates dynamics and enhances robustness of bimodal curli gene activation in escherichia coli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212085/
https://www.ncbi.nlm.nih.gov/pubmed/37186613
http://dx.doi.org/10.1371/journal.pgen.1010750
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