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A bistable prokaryotic differentiation system underlying development of conjugative transfer competence

The mechanisms and impact of horizontal gene transfer processes to distribute gene functions with potential adaptive benefit among prokaryotes have been well documented. In contrast, little is known about the life-style of mobile elements mediating horizontal gene transfer, whereas this is the ultim...

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Autores principales: Sulser, Sandra, Vucicevic, Andrea, Bellini, Veronica, Moritz, Roxane, Delavat, François, Sentchilo, Vladimir, Carraro, Nicolas, van der Meer, Jan Roelof
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9286271/
https://www.ncbi.nlm.nih.gov/pubmed/35763548
http://dx.doi.org/10.1371/journal.pgen.1010286
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author Sulser, Sandra
Vucicevic, Andrea
Bellini, Veronica
Moritz, Roxane
Delavat, François
Sentchilo, Vladimir
Carraro, Nicolas
van der Meer, Jan Roelof
author_facet Sulser, Sandra
Vucicevic, Andrea
Bellini, Veronica
Moritz, Roxane
Delavat, François
Sentchilo, Vladimir
Carraro, Nicolas
van der Meer, Jan Roelof
author_sort Sulser, Sandra
collection PubMed
description The mechanisms and impact of horizontal gene transfer processes to distribute gene functions with potential adaptive benefit among prokaryotes have been well documented. In contrast, little is known about the life-style of mobile elements mediating horizontal gene transfer, whereas this is the ultimate determinant for their transfer fitness. Here, we investigate the life-style of an integrative and conjugative element (ICE) within the genus Pseudomonas that is a model for a widespread family transmitting genes for xenobiotic compound metabolism and antibiotic resistances. Previous work showed bimodal ICE activation, but by using single cell time-lapse microscopy coupled to combinations of chromosomally integrated single copy ICE promoter-driven fluorescence reporters, RNA sequencing and mutant analysis, we now describe the complete regulon leading to the arisal of differentiated dedicated transfer competent cells. The regulon encompasses at least three regulatory nodes and five (possibly six) further conserved gene clusters on the ICE that all become expressed under stationary phase conditions. Time-lapse microscopy indicated expression of two regulatory nodes (i.e., bisR and alpA-bisDC) to precede that of the other clusters. Notably, expression of all clusters except of bisR was confined to the same cell subpopulation, and was dependent on the same key ICE regulatory factors. The ICE thus only transfers from a small fraction of cells in a population, with an estimated proportion of between 1.7–4%, which express various components of a dedicated transfer competence program imposed by the ICE, and form the centerpiece of ICE conjugation. The components mediating transfer competence are widely conserved, underscoring their selected fitness for efficient transfer of this class of mobile elements.
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spelling pubmed-92862712022-07-16 A bistable prokaryotic differentiation system underlying development of conjugative transfer competence Sulser, Sandra Vucicevic, Andrea Bellini, Veronica Moritz, Roxane Delavat, François Sentchilo, Vladimir Carraro, Nicolas van der Meer, Jan Roelof PLoS Genet Research Article The mechanisms and impact of horizontal gene transfer processes to distribute gene functions with potential adaptive benefit among prokaryotes have been well documented. In contrast, little is known about the life-style of mobile elements mediating horizontal gene transfer, whereas this is the ultimate determinant for their transfer fitness. Here, we investigate the life-style of an integrative and conjugative element (ICE) within the genus Pseudomonas that is a model for a widespread family transmitting genes for xenobiotic compound metabolism and antibiotic resistances. Previous work showed bimodal ICE activation, but by using single cell time-lapse microscopy coupled to combinations of chromosomally integrated single copy ICE promoter-driven fluorescence reporters, RNA sequencing and mutant analysis, we now describe the complete regulon leading to the arisal of differentiated dedicated transfer competent cells. The regulon encompasses at least three regulatory nodes and five (possibly six) further conserved gene clusters on the ICE that all become expressed under stationary phase conditions. Time-lapse microscopy indicated expression of two regulatory nodes (i.e., bisR and alpA-bisDC) to precede that of the other clusters. Notably, expression of all clusters except of bisR was confined to the same cell subpopulation, and was dependent on the same key ICE regulatory factors. The ICE thus only transfers from a small fraction of cells in a population, with an estimated proportion of between 1.7–4%, which express various components of a dedicated transfer competence program imposed by the ICE, and form the centerpiece of ICE conjugation. The components mediating transfer competence are widely conserved, underscoring their selected fitness for efficient transfer of this class of mobile elements. Public Library of Science 2022-06-28 /pmc/articles/PMC9286271/ /pubmed/35763548 http://dx.doi.org/10.1371/journal.pgen.1010286 Text en © 2022 Sulser et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sulser, Sandra
Vucicevic, Andrea
Bellini, Veronica
Moritz, Roxane
Delavat, François
Sentchilo, Vladimir
Carraro, Nicolas
van der Meer, Jan Roelof
A bistable prokaryotic differentiation system underlying development of conjugative transfer competence
title A bistable prokaryotic differentiation system underlying development of conjugative transfer competence
title_full A bistable prokaryotic differentiation system underlying development of conjugative transfer competence
title_fullStr A bistable prokaryotic differentiation system underlying development of conjugative transfer competence
title_full_unstemmed A bistable prokaryotic differentiation system underlying development of conjugative transfer competence
title_short A bistable prokaryotic differentiation system underlying development of conjugative transfer competence
title_sort bistable prokaryotic differentiation system underlying development of conjugative transfer competence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9286271/
https://www.ncbi.nlm.nih.gov/pubmed/35763548
http://dx.doi.org/10.1371/journal.pgen.1010286
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