The σB alternative sigma factor circuit modulates noise to generate different types of pulsing dynamics.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
08 2023
Historique:
received: 10 10 2022
accepted: 12 06 2023
revised: 16 08 2023
medline: 17 8 2023
pubmed: 4 8 2023
entrez: 4 8 2023
Statut: epublish

Résumé

Single-cell approaches are revealing a high degree of heterogeneity, or noise, in gene expression in isogenic bacteria. How gene circuits modulate this noise in gene expression to generate robust output dynamics is unclear. Here we use the Bacillus subtilis alternative sigma factor σB as a model system for understanding the role of noise in generating circuit output dynamics. σB controls the general stress response in B. subtilis and is activated by a range of energy and environmental stresses. Recent single-cell studies have revealed that the circuit can generate two distinct outputs, stochastic pulsing and a single pulse response, but the conditions under which each response is generated are under debate. We implement a stochastic mathematical model of the σB circuit to investigate this and find that the system's core circuit can generate both response types. This is despite one response (stochastic pulsing) being stochastic in nature, and the other (single response pulse) being deterministic. We demonstrate that the main determinant for whichever response is generated is the degree with which the input pathway activates the core circuit, although the noise properties of the input pathway also biases the system towards one or the other type of output. Thus, our work shows how stochastic modelling can reveal the mechanisms behind non-intuitive gene circuit output dynamics.

Identifiants

pubmed: 37540712
doi: 10.1371/journal.pcbi.1011265
pii: PCOMPBIOL-D-22-01479
pmc: PMC10431680
doi:

Substances chimiques

Sigma Factor 0
Bacterial Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011265

Informations de copyright

Copyright: © 2023 Loman, Locke. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Annu Rev Microbiol. 2008;62:193-210
pubmed: 18537474
J Bacteriol. 2012 Apr;194(7):1708-16
pubmed: 22287516
Can J Microbiol. 2017 Feb;63(2):89-99
pubmed: 28117604
J Bacteriol. 1996 Sep;178(18):5456-63
pubmed: 8808936
Rep Prog Phys. 2014;77(2):026601
pubmed: 24444693
Cell Syst. 2017 Jun 28;4(6):622-635.e9
pubmed: 28624615
Proc Natl Acad Sci U S A. 2013 Mar 5;110(10):4140-5
pubmed: 23407164
Nature. 2008 Aug 21;454(7207):987-90
pubmed: 18719588
Front Microbiol. 2020 Sep 15;11:1761
pubmed: 33042030
FEMS Microbiol Rev. 1998 Sep;22(3):127-50
pubmed: 9818380
PLoS Genet. 2017 Jul 20;13(7):e1006901
pubmed: 28727759
Annu Rev Phys Chem. 2007;58:35-55
pubmed: 17037977
Science. 2011 Oct 21;334(6054):366-9
pubmed: 21979936
Annu Rev Microbiol. 2003;57:441-66
pubmed: 14527287
Mol Microbiol. 2019 Aug;112(2):335-347
pubmed: 31119812
Nature. 2002 Sep 19;419(6904):304-8
pubmed: 12239569
J R Soc Interface. 2018 Apr;15(141):
pubmed: 29643226
Development. 2021 Feb 25;148(4):
pubmed: 33547135
BMC Bioinformatics. 2021 Nov 19;22(1):558
pubmed: 34798803
Nucleic Acids Res. 2018 Feb 28;46(4):2133-2144
pubmed: 29361130
Cell. 2011 Mar 18;144(6):910-25
pubmed: 21414483
mBio. 2022 Nov 21;13(6):e0200122
pubmed: 36409125
Drug Discov Today Dis Models. 2008 Winter;5(4):299-309
pubmed: 27840651
Cell. 2010 May 14;141(4):559-63
pubmed: 20478246
Nature. 2006 Mar 23;440(7083):545-50
pubmed: 16554821
Nucleic Acids Res. 2018 Aug 21;46(14):7450-7464
pubmed: 29986061
Phys Rev Lett. 2006 Oct 20;97(16):168302
pubmed: 17155441
Mol Syst Biol. 2021 Jul;17(7):e9832
pubmed: 34286912
J Mol Biol. 1996 Jul 12;260(2):165-77
pubmed: 8764398
Annu Rev Microbiol. 2007;61:215-36
pubmed: 18035607
Microbiology (Reading). 2012 Mar;158(Pt 3):696-707
pubmed: 22174379
Phys Rev E Stat Nonlin Soft Matter Phys. 2011 Jun;83(6 Pt 1):061904
pubmed: 21797400
Curr Biol. 2016 May 9;26(9):1138-47
pubmed: 27068419
Annu Rev Cell Dev Biol. 2009;25:301-27
pubmed: 19575655
Discrete Continuous Dyn Syst Ser B. 2017;22(7):2731-2761
pubmed: 29527134
Phys Rev E. 2020 Mar;101(3-1):032403
pubmed: 32290003
Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2330-4
pubmed: 8460143
J R Soc Interface. 2019 Feb 28;16(151):20180943
pubmed: 30958205
Mol Syst Biol. 2016 May 23;12(5):871
pubmed: 27216630
PLoS Comput Biol. 2020 Mar 16;16(3):e1007671
pubmed: 32176683
Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):814-9
pubmed: 9023339
J Bacteriol. 1990 Oct;172(10):5575-85
pubmed: 2170324
Nature. 2002 Nov 14;420(6912):231-7
pubmed: 12432408
Nat Commun. 2020 Feb 19;11(1):950
pubmed: 32075967
Science. 2002 Aug 16;297(5584):1183-6
pubmed: 12183631
J Bacteriol. 1994 Apr;176(7):1813-20
pubmed: 8144446
Cell Syst. 2018 Feb 28;6(2):216-229.e15
pubmed: 29454936
Mol Syst Biol. 2008;4:196
pubmed: 18463620
J Bacteriol. 1995 Jan;177(1):123-33
pubmed: 8002610
PLoS Comput Biol. 2016 Oct 21;12(10):e1005154
pubmed: 27768683
Cell. 2005 Dec 16;123(6):1025-36
pubmed: 16360033
Nat Commun. 2018 Dec 17;9(1):5333
pubmed: 30559445
Nat Commun. 2019 Jun 27;10(1):2835
pubmed: 31249377
PLoS Comput Biol. 2016 Dec 15;12(12):e1005267
pubmed: 27977677
PLoS Comput Biol. 2012;8(8):e1002672
pubmed: 22956903
Annu Rev Microbiol. 2014;68:357-76
pubmed: 25002089
Cell Syst. 2018 Apr 25;6(4):521-530.e3
pubmed: 29574056
Mol Syst Biol. 2013 Oct 29;9:702
pubmed: 24169405
Mol Microbiol. 2000 Jan;35(1):180-8
pubmed: 10632888
IET Syst Biol. 2012 Aug;6(4):102-15
pubmed: 23039691
Nat Commun. 2018 Aug 30;9(1):3521
pubmed: 30166548
J Bacteriol. 1992 Feb;174(3):749-57
pubmed: 1732211
J R Soc Interface. 2020 Jul;17(168):20200360
pubmed: 32634365
Mol Syst Biol. 2006;2:58
pubmed: 17102803
Nat Protoc. 2011 Dec 15;7(1):80-8
pubmed: 22179594
Physiol Genomics. 2012 Jun 1;44(11):607-21
pubmed: 22510707

Auteurs

Torkel E Loman (TE)

Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom.

James C W Locke (JCW)

Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom.

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Classifications MeSH