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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...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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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. |
format | Online Article Text |
id | pubmed-9286271 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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