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An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element

Conjugative transfer of the integrative and conjugative element ICEclc in Pseudomonas requires development of a transfer competence state in stationary phase, which arises only in 3–5% of individual cells. The mechanisms controlling this bistable switch between non-active and transfer competent cell...

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Autores principales: Carraro, Nicolas, Richard, Xavier, Sulser, Sandra, Delavat, François, Mazza, Christian, van der Meer, Jan Roelof
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423338/
https://www.ncbi.nlm.nih.gov/pubmed/32720896
http://dx.doi.org/10.7554/eLife.57915
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author Carraro, Nicolas
Richard, Xavier
Sulser, Sandra
Delavat, François
Mazza, Christian
van der Meer, Jan Roelof
author_facet Carraro, Nicolas
Richard, Xavier
Sulser, Sandra
Delavat, François
Mazza, Christian
van der Meer, Jan Roelof
author_sort Carraro, Nicolas
collection PubMed
description Conjugative transfer of the integrative and conjugative element ICEclc in Pseudomonas requires development of a transfer competence state in stationary phase, which arises only in 3–5% of individual cells. The mechanisms controlling this bistable switch between non-active and transfer competent cells have long remained enigmatic. Using a variety of genetic tools and epistasis experiments in P. putida, we uncovered an ‘upstream’ cascade of three consecutive transcription factor-nodes, which controls transfer competence initiation. One of the uncovered transcription factors (named BisR) is representative for a new regulator family. Initiation activates a feedback loop, controlled by a second hitherto unrecognized heteromeric transcription factor named BisDC. Stochastic modelling and experimental data demonstrated the feedback loop to act as a scalable converter of unimodal (population-wide or ‘analog’) input to bistable (subpopulation-specific or ‘digital’) output. The feedback loop further enables prolonged production of BisDC, which ensures expression of the ‘downstream’ functions mediating ICE transfer competence in activated cells. Phylogenetic analyses showed that the ICEclc regulatory constellation with BisR and BisDC is widespread among Gamma- and Beta-proteobacteria, including various pathogenic strains, highlighting its evolutionary conservation and prime importance to control the behaviour of this wide family of conjugative elements.
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spelling pubmed-74233382020-08-13 An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element Carraro, Nicolas Richard, Xavier Sulser, Sandra Delavat, François Mazza, Christian van der Meer, Jan Roelof eLife Genetics and Genomics Conjugative transfer of the integrative and conjugative element ICEclc in Pseudomonas requires development of a transfer competence state in stationary phase, which arises only in 3–5% of individual cells. The mechanisms controlling this bistable switch between non-active and transfer competent cells have long remained enigmatic. Using a variety of genetic tools and epistasis experiments in P. putida, we uncovered an ‘upstream’ cascade of three consecutive transcription factor-nodes, which controls transfer competence initiation. One of the uncovered transcription factors (named BisR) is representative for a new regulator family. Initiation activates a feedback loop, controlled by a second hitherto unrecognized heteromeric transcription factor named BisDC. Stochastic modelling and experimental data demonstrated the feedback loop to act as a scalable converter of unimodal (population-wide or ‘analog’) input to bistable (subpopulation-specific or ‘digital’) output. The feedback loop further enables prolonged production of BisDC, which ensures expression of the ‘downstream’ functions mediating ICE transfer competence in activated cells. Phylogenetic analyses showed that the ICEclc regulatory constellation with BisR and BisDC is widespread among Gamma- and Beta-proteobacteria, including various pathogenic strains, highlighting its evolutionary conservation and prime importance to control the behaviour of this wide family of conjugative elements. eLife Sciences Publications, Ltd 2020-07-28 /pmc/articles/PMC7423338/ /pubmed/32720896 http://dx.doi.org/10.7554/eLife.57915 Text en © 2020, Carraro et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Genetics and Genomics
Carraro, Nicolas
Richard, Xavier
Sulser, Sandra
Delavat, François
Mazza, Christian
van der Meer, Jan Roelof
An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
title An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
title_full An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
title_fullStr An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
title_full_unstemmed An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
title_short An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
title_sort analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element
topic Genetics and Genomics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423338/
https://www.ncbi.nlm.nih.gov/pubmed/32720896
http://dx.doi.org/10.7554/eLife.57915
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