Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships

ABSTRACT Escherichia coli uses two-component systems (TCSs) to respond to environmental signals. TCSs affect gene expression and are parts of E. coli’s global transcriptional regulatory network (TRN). Here, we identified the regulons of five TCSs in E. coli MG1655: BaeSR and CpxAR, which were stimul...

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Autores principales:	Kumari Sonal Choudhary, Julia A. Kleinmanns, Katherine Decker, Anand V. Sastry, Ye Gao, Richard Szubin, Yara Seif, Bernhard O. Palsson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	two-component systems E. coli independent component analysis transcriptomics ChIP-exo transcriptional regulatory network Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1d09b6685d1e4e5686f142e03c9dcd78
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spelling	oai:doaj.org-article:1d09b6685d1e4e5686f142e03c9dcd782021-12-02T19:47:38ZElucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships10.1128/mSystems.00980-202379-5077https://doaj.org/article/1d09b6685d1e4e5686f142e03c9dcd782020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00980-20https://doaj.org/toc/2379-5077ABSTRACT Escherichia coli uses two-component systems (TCSs) to respond to environmental signals. TCSs affect gene expression and are parts of E. coli’s global transcriptional regulatory network (TRN). Here, we identified the regulons of five TCSs in E. coli MG1655: BaeSR and CpxAR, which were stimulated by ethanol stress; KdpDE and PhoRB, induced by limiting potassium and phosphate, respectively; and ZraSR, stimulated by zinc. We analyzed RNA-seq data using independent component analysis (ICA). ChIP-exo data were used to validate condition-specific target gene binding sites. Based on these data, we do the following: (i) identify the target genes for each TCS; (ii) show how the target genes are transcribed in response to stimulus; and (iii) reveal novel relationships between TCSs, which indicate noncognate inducers for various response regulators, such as BaeR to iron starvation, CpxR to phosphate limitation, and PhoB and ZraR to cell envelope stress. Our understanding of the TRN in E. coli is thus notably expanded. IMPORTANCE E. coli is a common commensal microbe found in the human gut microenvironment; however, some strains cause diseases like diarrhea, urinary tract infections, and meningitis. E. coli’s two-component systems (TCSs) modulate target gene expression, especially related to virulence, pathogenesis, and antimicrobial peptides, in response to environmental stimuli. Thus, it is of utmost importance to understand the transcriptional regulation of TCSs to infer bacterial environmental adaptation and disease pathogenicity. Utilizing a combinatorial approach integrating RNA sequencing (RNA-seq), independent component analysis, chromatin immunoprecipitation coupled with exonuclease treatment (ChIP-exo), and data mining, we suggest five different modes of TCS transcriptional regulation. Our data further highlight noncognate inducers of TCSs, which emphasizes the cross-regulatory nature of TCSs in E. coli and suggests that TCSs may have a role beyond their cognate functionalities. In summary, these results can lead to an understanding of the metabolic capabilities of bacteria and correctly predict complex phenotype under diverse conditions, especially when further incorporated with genome-scale metabolic models.Kumari Sonal ChoudharyJulia A. KleinmannsKatherine DeckerAnand V. SastryYe GaoRichard SzubinYara SeifBernhard O. PalssonAmerican Society for Microbiologyarticletwo-component systemsE. coliindependent component analysistranscriptomicsChIP-exotranscriptional regulatory networkMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	two-component systems E. coli independent component analysis transcriptomics ChIP-exo transcriptional regulatory network Microbiology QR1-502
spellingShingle	two-component systems E. coli independent component analysis transcriptomics ChIP-exo transcriptional regulatory network Microbiology QR1-502 Kumari Sonal Choudhary Julia A. Kleinmanns Katherine Decker Anand V. Sastry Ye Gao Richard Szubin Yara Seif Bernhard O. Palsson Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships
description	ABSTRACT Escherichia coli uses two-component systems (TCSs) to respond to environmental signals. TCSs affect gene expression and are parts of E. coli’s global transcriptional regulatory network (TRN). Here, we identified the regulons of five TCSs in E. coli MG1655: BaeSR and CpxAR, which were stimulated by ethanol stress; KdpDE and PhoRB, induced by limiting potassium and phosphate, respectively; and ZraSR, stimulated by zinc. We analyzed RNA-seq data using independent component analysis (ICA). ChIP-exo data were used to validate condition-specific target gene binding sites. Based on these data, we do the following: (i) identify the target genes for each TCS; (ii) show how the target genes are transcribed in response to stimulus; and (iii) reveal novel relationships between TCSs, which indicate noncognate inducers for various response regulators, such as BaeR to iron starvation, CpxR to phosphate limitation, and PhoB and ZraR to cell envelope stress. Our understanding of the TRN in E. coli is thus notably expanded. IMPORTANCE E. coli is a common commensal microbe found in the human gut microenvironment; however, some strains cause diseases like diarrhea, urinary tract infections, and meningitis. E. coli’s two-component systems (TCSs) modulate target gene expression, especially related to virulence, pathogenesis, and antimicrobial peptides, in response to environmental stimuli. Thus, it is of utmost importance to understand the transcriptional regulation of TCSs to infer bacterial environmental adaptation and disease pathogenicity. Utilizing a combinatorial approach integrating RNA sequencing (RNA-seq), independent component analysis, chromatin immunoprecipitation coupled with exonuclease treatment (ChIP-exo), and data mining, we suggest five different modes of TCS transcriptional regulation. Our data further highlight noncognate inducers of TCSs, which emphasizes the cross-regulatory nature of TCSs in E. coli and suggests that TCSs may have a role beyond their cognate functionalities. In summary, these results can lead to an understanding of the metabolic capabilities of bacteria and correctly predict complex phenotype under diverse conditions, especially when further incorporated with genome-scale metabolic models.
format	article
author	Kumari Sonal Choudhary Julia A. Kleinmanns Katherine Decker Anand V. Sastry Ye Gao Richard Szubin Yara Seif Bernhard O. Palsson
author_facet	Kumari Sonal Choudhary Julia A. Kleinmanns Katherine Decker Anand V. Sastry Ye Gao Richard Szubin Yara Seif Bernhard O. Palsson
author_sort	Kumari Sonal Choudhary
title	Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships
title_short	Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships
title_full	Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships
title_fullStr	Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships
title_full_unstemmed	Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships
title_sort	elucidation of regulatory modes for five two-component systems in <named-content content-type="genus-species">escherichia coli</named-content> reveals novel relationships
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/1d09b6685d1e4e5686f142e03c9dcd78
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Elucidation of Regulatory Modes for Five Two-Component Systems in <named-content content-type="genus-species">Escherichia coli</named-content> Reveals Novel Relationships

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