Frequency modulation of a bacterial quorum sensing response.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
19 05 2022
Historique:
received: 21 10 2021
accepted: 21 04 2022
entrez: 19 5 2022
pubmed: 20 5 2022
medline: 24 5 2022
Statut: epublish

Résumé

In quorum sensing, bacteria secrete or release small molecules into the environment that, once they reach a certain threshold, trigger a behavioural change in the population. As the concentration of these so-called autoinducers is supposed to reflect population density, they were originally assumed to be continuously produced by all cells in a population. However, here we show that in the α-proteobacterium Sinorhizobium meliloti expression of the autoinducer synthase gene is realized in asynchronous stochastic pulses that result from scarcity and, presumably, low binding affinity of the key activator. Physiological cues modulate pulse frequency, and pulse frequency in turn modulates the velocity with which autoinducer levels in the environment reach the threshold to trigger the quorum sensing response. We therefore propose that frequency-modulated pulsing in S. meliloti represents the molecular mechanism for a collective decision-making process in which each cell's physiological state and need for behavioural adaptation is encoded in the pulse frequency with which it expresses the autoinducer synthase gene; the pulse frequencies of all members of the population are then integrated in the common pool of autoinducers, and only once this vote crosses the threshold, the response behaviour is initiated.

Identifiants

pubmed: 35589697
doi: 10.1038/s41467-022-30307-6
pii: 10.1038/s41467-022-30307-6
pmc: PMC9120067
doi:

Substances chimiques

Bacterial Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2772

Informations de copyright

© 2022. The Author(s).

Références

J Bacteriol. 2012 Apr;194(8):2027-35
pubmed: 22328673
Science. 2011 Oct 21;334(6054):366-9
pubmed: 21979936
J Bacteriol. 1994 Jan;176(2):269-75
pubmed: 8288518
Mol Microbiol. 2019 Aug;112(2):678-698
pubmed: 31124196
J Bacteriol. 1991 Nov;173(22):7391-4
pubmed: 1938929
J Bacteriol. 2013 Nov;195(22):5051-63
pubmed: 23995643
Proc Biol Sci. 2014 Apr 16;281(1784):20132575
pubmed: 24741008
Genes (Basel). 2018 May 18;9(5):
pubmed: 29783703
Nature. 2010 Sep 9;467(7312):167-73
pubmed: 20829787
Mol Microbiol. 2009 Dec;74(5):1238-56
pubmed: 19889097
Nature. 2011 Jul 20;475(7356):308-15
pubmed: 21776076
J Bacteriol. 2002 Sep;184(18):5067-76
pubmed: 12193623
Appl Environ Microbiol. 2011 Sep;77(17):6286-9
pubmed: 21724873
J Bacteriol. 2007 Jul;189(13):4827-36
pubmed: 17449617
Nat Rev Microbiol. 2007 Mar;5(3):230-9
pubmed: 17304251
Science. 2010 Jul 30;329(5991):533-8
pubmed: 20671182
J Biotechnol. 2015 Mar 20;198:3-14
pubmed: 25661839
Nat Methods. 2019 Dec;16(12):1226-1232
pubmed: 31570887
Microbiol Mol Biol Rev. 2015 Mar;79(1):153-69
pubmed: 25694124
Nat Commun. 2017 Oct 11;8(1):854
pubmed: 29021534
J Bacteriol. 1988 Sep;170(9):4040-6
pubmed: 3410823
Nat Commun. 2015 Jan 16;6:5945
pubmed: 25592773
Trends Cogn Sci. 2009 Jan;13(1):36-43
pubmed: 19058992
Science. 2013 Dec 6;342(6163):1193-200
pubmed: 24311681
PLoS One. 2012;7(8):e42611
pubmed: 22912712
Trends Genet. 2020 Apr;36(4):288-297
pubmed: 32035656
Science. 2006 Mar 17;311(5767):1600-3
pubmed: 16543458
Chaos. 2018 Oct;28(10):106316
pubmed: 30384658
Nature. 2006 Mar 16;440(7082):358-62
pubmed: 16541077
Appl Environ Microbiol. 2015 Aug 15;81(16):5280-9
pubmed: 26025903
Nat Struct Mol Biol. 2011 Dec 18;19(1):31-9
pubmed: 22179789
Nature. 2008 Sep 25;455(7212):485-90
pubmed: 18818649
Nature. 2014 Oct 16;514(7522):376-9
pubmed: 25186725
Cell Syst. 2018 Apr 25;6(4):496-507.e6
pubmed: 29655705
Curr Biol. 2014 Sep 22;24(18):2189-2194
pubmed: 25220054
J Bacteriol. 1970 Oct;104(1):313-22
pubmed: 5473898
Science. 2002 Aug 16;297(5584):1183-6
pubmed: 12183631
J Bacteriol. 2013 Jul;195(14):3224-36
pubmed: 23687265
Cell Syst. 2018 Feb 28;6(2):216-229.e15
pubmed: 29454936
Appl Environ Microbiol. 2014 Sep;80(18):5572-82
pubmed: 25002427
Nat Rev Microbiol. 2016 Aug 11;14(9):563-75
pubmed: 27510863
J R Soc Interface. 2015 Feb 6;12(103):
pubmed: 25505130
EMBO J. 1990 Apr;9(4):973-9
pubmed: 2182324
J Bacteriol. 1985 Nov;164(2):918-21
pubmed: 2997137
Cell. 2008 Oct 17;135(2):216-26
pubmed: 18957198
J Bacteriol. 1985 Oct;164(1):45-50
pubmed: 2995319
J Exp Biol. 2008 Dec;211(Pt 23):3691-7
pubmed: 19011208
Nat Rev Microbiol. 2008 Mar;6(3):199-210
pubmed: 18264116
J Mol Biol. 2019 Nov 22;431(23):4530-4546
pubmed: 31051177
Sensors (Basel). 2012;12(4):4156-71
pubmed: 22666024
Trends Microbiol. 2010 Sep;18(9):383-7
pubmed: 20573513
Anal Bioanal Chem. 2007 Jan;387(2):391-8
pubmed: 16953316
Genes Dev. 2001 Jun 15;15(12):1468-80
pubmed: 11410527
Mol Microbiol. 2014 May;92(3):557-69
pubmed: 24601980
Proc Natl Acad Sci U S A. 1972 May;69(5):1073-6
pubmed: 4338581
FEMS Microbiol Ecol. 2009 Oct;70(1):1-19
pubmed: 19689448
J Bacteriol. 2015 Nov 16;198(3):521-35
pubmed: 26574513
Trends Microbiol. 2002 Aug;10(8):365-70
pubmed: 12160634
Nucleus. 2018 Jan 1;9(1):149-160
pubmed: 29285985
Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4832-7
pubmed: 10220379
Nat Protoc. 2011 Dec 15;7(1):80-8
pubmed: 22179594
J Bacteriol. 2015 Jul;197(13):2139-2149
pubmed: 25897034
Mol Microbiol. 2005 Jan;55(2):526-45
pubmed: 15659168
Nucleic Acids Res. 1997 Mar 15;25(6):1203-10
pubmed: 9092630

Auteurs

Vera Bettenworth (V)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany. vera.bettenworth@gmx.de.
Department of Biology, Philipps-Universität Marburg, Marburg, Germany. vera.bettenworth@gmx.de.

Simon van Vliet (S)

Biozentrum, University of Basel, Basel, Switzerland.

Bartosz Turkowyd (B)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany.
Max Planck Institute for Terrestrial Microbiology, Marburg, Germany.
Department of Physics, Carnegie Mellon University, Pittsburgh, PA, USA.
Institut für Mikrobiologie und Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany.

Annika Bamberger (A)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany.
Department of Biology, Philipps-Universität Marburg, Marburg, Germany.

Heiko Wendt (H)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany.
Department of Biology, Philipps-Universität Marburg, Marburg, Germany.

Matthew McIntosh (M)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany.
Department of Biology, Philipps-Universität Marburg, Marburg, Germany.
Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Gießen, Gießen, Germany.

Wieland Steinchen (W)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany.
Department of Chemistry, Philipps-Universität Marburg, Marburg, Germany.

Ulrike Endesfelder (U)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany.
Max Planck Institute for Terrestrial Microbiology, Marburg, Germany.
Department of Physics, Carnegie Mellon University, Pittsburgh, PA, USA.
Institut für Mikrobiologie und Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany.

Anke Becker (A)

Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany. anke.becker@synmikro.uni-marburg.de.
Department of Biology, Philipps-Universität Marburg, Marburg, Germany. anke.becker@synmikro.uni-marburg.de.

Articles similaires

Photosynthesis Ribulose-Bisphosphate Carboxylase Carbon Dioxide Molecular Dynamics Simulation Cyanobacteria
Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial

Classifications MeSH