Sequence-dependent model of genes with dual σ factor preference

Ines S.C. Baptista; Vinodh Kandavalli; Vatsala Chauhan; Mohamed N.M. Bahrudeen; Bilena L.B. Almeida; Cristina S.D. Palma; Suchintak Dash; Andre S. Ribeiro

doi:10.1016/j.bbagrm.2022.194812

Sequence-dependent model of genes with dual σ factor preference

Ines S.C. Baptista, Vinodh Kandavalli, Vatsala Chauhan, Mohamed N.M. Bahrudeen, Bilena L.B. Almeida, Cristina S.D. Palma, Suchintak Dash, Andre S. Ribeiro

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Abstract

Escherichia coli uses σ factors to quickly control large gene cohorts during stress conditions. While most of its genes respond to a single σ factor, approximately 5% of them have dual σ factor preference. The most common are those responsive to both σ⁷⁰, which controls housekeeping genes, and σ³⁸, which activates genes during stationary growth and stresses. Using RNA-seq and flow-cytometry measurements, we show that ‘σ⁷⁰⁺³⁸ genes’ are nearly as upregulated in stationary growth as ‘σ³⁸ genes’. Moreover, we find a clear quantitative relationship between their promoter sequence and their response strength to changes in σ³⁸ levels. We then propose and validate a sequence dependent model of σ⁷⁰⁺³⁸ genes, with dual sensitivity to σ³⁸ and σ⁷⁰, that is applicable in the exponential and stationary growth phases, as well in the transient period in between. We further propose a general model, applicable to other stresses and σ factor combinations. Given this, promoters controlling σ⁷⁰⁺³⁸ genes (and variants) could become important building blocks of synthetic circuits with predictable, sequence-dependent sensitivity to transitions between the exponential and stationary growth phases.

Original language	English
Article number	194812
Journal	Biochimica et Biophysica Acta - Gene Regulatory Mechanisms
Volume	1865
Issue number	3
DOIs	https://doi.org/10.1016/j.bbagrm.2022.194812
Publication status	Published - Apr 2022
Publication type	A1 Journal article-refereed

Keywords

Dual σ factor preference
E. coli
Flow cytometry
RNA-seq
Sequence-dependent gene expression model

Publication forum classification

Publication forum level 1

ASJC Scopus subject areas

Biophysics
Structural Biology
Biochemistry
Molecular Biology
Genetics

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10.1016/j.bbagrm.2022.194812

1-s2.0-S187493992200027X-mainFinal published version, 3.27 MBLicence: CC BY

https://urn.fi/URN:NBN:fi:tuni-202204253523Licence: CC BY

Sequence-dependent model of genes with dual σ factor preference
Calado Baptista, I. (Creator), Kandavalli, V. (Creator), Chauhan, V. (Creator), Mohamed Bahrudeen, M. N. (Creator), Lima de Brito Almeida, B. (Creator), Palma, C. (Creator), Dash, S. (Creator) & Sanches Ribeiro, A. (Creator), Dryad, 11 Apr 2022
DOI: 10.5061/dryad.jsxksn0b7, https://zenodo.org/record/6450355
Dataset

Cite this

@article{243ad80b689d4e4e833ee7e26ff08d03,

title = "Sequence-dependent model of genes with dual σ factor preference",

abstract = "Escherichia coli uses σ factors to quickly control large gene cohorts during stress conditions. While most of its genes respond to a single σ factor, approximately 5% of them have dual σ factor preference. The most common are those responsive to both σ70, which controls housekeeping genes, and σ38, which activates genes during stationary growth and stresses. Using RNA-seq and flow-cytometry measurements, we show that {\textquoteleft}σ70+38 genes{\textquoteright} are nearly as upregulated in stationary growth as {\textquoteleft}σ38 genes{\textquoteright}. Moreover, we find a clear quantitative relationship between their promoter sequence and their response strength to changes in σ38 levels. We then propose and validate a sequence dependent model of σ70+38 genes, with dual sensitivity to σ38 and σ70, that is applicable in the exponential and stationary growth phases, as well in the transient period in between. We further propose a general model, applicable to other stresses and σ factor combinations. Given this, promoters controlling σ70+38 genes (and variants) could become important building blocks of synthetic circuits with predictable, sequence-dependent sensitivity to transitions between the exponential and stationary growth phases.",

keywords = "Dual σ factor preference, E. coli, Flow cytometry, RNA-seq, Sequence-dependent gene expression model",

author = "Baptista, {Ines S.C.} and Vinodh Kandavalli and Vatsala Chauhan and Bahrudeen, {Mohamed N.M.} and Almeida, {Bilena L.B.} and Palma, {Cristina S.D.} and Suchintak Dash and Ribeiro, {Andre S.}",

note = "Funding Information: This work was supported by the Jane and Aatos Erkko Foundation [ 10-10524-38 to A.S.R]; Finnish Cultural Foundation [ 00200193 and 00212591 to I.S.C.B., and 50201300 to S.D.]; Pirkanmaa Regional Fund of the Finnish Cultural Foundation to V.K.; Suomalainen Tiedeakatemia to C.S.D.P.; Tampere University Graduate Program to V.C., M.N.M.B., and B.L.B.A.; EDUFI Fellowship [TM-19-11105 to S.D]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: {\textcopyright} 2022 The Authors Preprint available https://doi.org/10.1101/2021.11.17.468920",

year = "2022",

month = apr,

doi = "10.1016/j.bbagrm.2022.194812",

language = "English",

volume = "1865",

journal = "Biochimica et Biophysica Acta - Gene Regulatory Mechanisms",

issn = "1874-9399",

publisher = "Elsevier",

number = "3",

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TY - JOUR

T1 - Sequence-dependent model of genes with dual σ factor preference

AU - Baptista, Ines S.C.

AU - Kandavalli, Vinodh

AU - Chauhan, Vatsala

AU - Bahrudeen, Mohamed N.M.

AU - Almeida, Bilena L.B.

AU - Palma, Cristina S.D.

AU - Dash, Suchintak

AU - Ribeiro, Andre S.

N1 - Funding Information: This work was supported by the Jane and Aatos Erkko Foundation [ 10-10524-38 to A.S.R]; Finnish Cultural Foundation [ 00200193 and 00212591 to I.S.C.B., and 50201300 to S.D.]; Pirkanmaa Regional Fund of the Finnish Cultural Foundation to V.K.; Suomalainen Tiedeakatemia to C.S.D.P.; Tampere University Graduate Program to V.C., M.N.M.B., and B.L.B.A.; EDUFI Fellowship [TM-19-11105 to S.D]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: © 2022 The Authors Preprint available https://doi.org/10.1101/2021.11.17.468920

PY - 2022/4

Y1 - 2022/4

N2 - Escherichia coli uses σ factors to quickly control large gene cohorts during stress conditions. While most of its genes respond to a single σ factor, approximately 5% of them have dual σ factor preference. The most common are those responsive to both σ70, which controls housekeeping genes, and σ38, which activates genes during stationary growth and stresses. Using RNA-seq and flow-cytometry measurements, we show that ‘σ70+38 genes’ are nearly as upregulated in stationary growth as ‘σ38 genes’. Moreover, we find a clear quantitative relationship between their promoter sequence and their response strength to changes in σ38 levels. We then propose and validate a sequence dependent model of σ70+38 genes, with dual sensitivity to σ38 and σ70, that is applicable in the exponential and stationary growth phases, as well in the transient period in between. We further propose a general model, applicable to other stresses and σ factor combinations. Given this, promoters controlling σ70+38 genes (and variants) could become important building blocks of synthetic circuits with predictable, sequence-dependent sensitivity to transitions between the exponential and stationary growth phases.

AB - Escherichia coli uses σ factors to quickly control large gene cohorts during stress conditions. While most of its genes respond to a single σ factor, approximately 5% of them have dual σ factor preference. The most common are those responsive to both σ70, which controls housekeeping genes, and σ38, which activates genes during stationary growth and stresses. Using RNA-seq and flow-cytometry measurements, we show that ‘σ70+38 genes’ are nearly as upregulated in stationary growth as ‘σ38 genes’. Moreover, we find a clear quantitative relationship between their promoter sequence and their response strength to changes in σ38 levels. We then propose and validate a sequence dependent model of σ70+38 genes, with dual sensitivity to σ38 and σ70, that is applicable in the exponential and stationary growth phases, as well in the transient period in between. We further propose a general model, applicable to other stresses and σ factor combinations. Given this, promoters controlling σ70+38 genes (and variants) could become important building blocks of synthetic circuits with predictable, sequence-dependent sensitivity to transitions between the exponential and stationary growth phases.

KW - Dual σ factor preference

KW - E. coli

KW - Flow cytometry

KW - RNA-seq

KW - Sequence-dependent gene expression model

U2 - 10.1016/j.bbagrm.2022.194812

DO - 10.1016/j.bbagrm.2022.194812

M3 - Article

C2 - 35338024

SN - 1874-9399

VL - 1865

JO - Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

JF - Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

IS - 3

M1 - 194812

ER -

Sequence-dependent model of genes with dual σ factor preference

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Sequence-dependent model of genes with dual σ factor preference

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