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The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli

The gene expression state of exponentially growing Escherichia coli cells is manifested by high expression of essential and growth-associated genes and low levels of stress-related and horizontally acquired genes. An important player in maintaining this homeostasis is the H-NS-StpA gene silencing sy...

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Autores principales: Srinivasan, Rajalakshmi, Scolari, Vittore Ferdinando, Lagomarsino, Marco Cosentino, Seshasayee, Aswin Sai Narain
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4288151/
https://www.ncbi.nlm.nih.gov/pubmed/25429971
http://dx.doi.org/10.1093/nar/gku1229
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author Srinivasan, Rajalakshmi
Scolari, Vittore Ferdinando
Lagomarsino, Marco Cosentino
Seshasayee, Aswin Sai Narain
author_facet Srinivasan, Rajalakshmi
Scolari, Vittore Ferdinando
Lagomarsino, Marco Cosentino
Seshasayee, Aswin Sai Narain
author_sort Srinivasan, Rajalakshmi
collection PubMed
description The gene expression state of exponentially growing Escherichia coli cells is manifested by high expression of essential and growth-associated genes and low levels of stress-related and horizontally acquired genes. An important player in maintaining this homeostasis is the H-NS-StpA gene silencing system. A Δhns-stpA deletion mutant results in high expression of otherwise-silent horizontally acquired genes, many located in the terminus-half of the chromosome, and an indirect downregulation of many highly expressed genes. The Δhns-stpA double mutant displays slow growth. Using laboratory evolution we address the evolutionary strategies that E. coli would adopt to redress this gene expression imbalance. We show that two global gene regulatory mutations—(i) point mutations inactivating the stress-responsive sigma factor RpoS or σ38 and (ii) an amplification of ∼40% of the chromosome centred around the origin of replication—converge in partially reversing the global gene expression imbalance caused by Δhns-stpA. Transcriptome data of these mutants further show a three-way link amongst the global gene regulatory networks of H-NS and σ38, as well as chromosome architecture. Increasing gene expression around the terminus of replication results in a decrease in the expression of genes around the origin and vice versa; this appears to be a persistent phenomenon observed as an association across ∼300 publicly-available gene expression data sets for E. coli. These global suppressor effects are transient and rapidly give way to more specific mutations, whose roles in reversing the growth defect of H-NS mutations remain to be understood.
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spelling pubmed-42881512015-02-19 The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli Srinivasan, Rajalakshmi Scolari, Vittore Ferdinando Lagomarsino, Marco Cosentino Seshasayee, Aswin Sai Narain Nucleic Acids Res Genomics The gene expression state of exponentially growing Escherichia coli cells is manifested by high expression of essential and growth-associated genes and low levels of stress-related and horizontally acquired genes. An important player in maintaining this homeostasis is the H-NS-StpA gene silencing system. A Δhns-stpA deletion mutant results in high expression of otherwise-silent horizontally acquired genes, many located in the terminus-half of the chromosome, and an indirect downregulation of many highly expressed genes. The Δhns-stpA double mutant displays slow growth. Using laboratory evolution we address the evolutionary strategies that E. coli would adopt to redress this gene expression imbalance. We show that two global gene regulatory mutations—(i) point mutations inactivating the stress-responsive sigma factor RpoS or σ38 and (ii) an amplification of ∼40% of the chromosome centred around the origin of replication—converge in partially reversing the global gene expression imbalance caused by Δhns-stpA. Transcriptome data of these mutants further show a three-way link amongst the global gene regulatory networks of H-NS and σ38, as well as chromosome architecture. Increasing gene expression around the terminus of replication results in a decrease in the expression of genes around the origin and vice versa; this appears to be a persistent phenomenon observed as an association across ∼300 publicly-available gene expression data sets for E. coli. These global suppressor effects are transient and rapidly give way to more specific mutations, whose roles in reversing the growth defect of H-NS mutations remain to be understood. Oxford University Press 2015-01-09 2014-11-27 /pmc/articles/PMC4288151/ /pubmed/25429971 http://dx.doi.org/10.1093/nar/gku1229 Text en © The Author(s) 2014. Published by Oxford University Press on behalf of Nucleic Acids Research. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Genomics
Srinivasan, Rajalakshmi
Scolari, Vittore Ferdinando
Lagomarsino, Marco Cosentino
Seshasayee, Aswin Sai Narain
The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli
title The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli
title_full The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli
title_fullStr The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli
title_full_unstemmed The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli
title_short The genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in Escherichia coli
title_sort genome-scale interplay amongst xenogene silencing, stress response and chromosome architecture in escherichia coli
topic Genomics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4288151/
https://www.ncbi.nlm.nih.gov/pubmed/25429971
http://dx.doi.org/10.1093/nar/gku1229
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