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An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13

The integrative and conjugative element ICEclc is a mobile genetic element in Pseudomonas knackmussii B13, and an experimental model for a widely distributed group of elements in Proteobacteria. ICEclc is transferred from specialized transfer competent cells, which arise at a frequency of 3-5% in a...

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Autores principales: Pradervand, Nicolas, Sulser, Sandra, Delavat, François, Miyazaki, Ryo, Lamas, Iker, van der Meer, Jan Roelof
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063739/
https://www.ncbi.nlm.nih.gov/pubmed/24945944
http://dx.doi.org/10.1371/journal.pgen.1004441
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author Pradervand, Nicolas
Sulser, Sandra
Delavat, François
Miyazaki, Ryo
Lamas, Iker
van der Meer, Jan Roelof
author_facet Pradervand, Nicolas
Sulser, Sandra
Delavat, François
Miyazaki, Ryo
Lamas, Iker
van der Meer, Jan Roelof
author_sort Pradervand, Nicolas
collection PubMed
description The integrative and conjugative element ICEclc is a mobile genetic element in Pseudomonas knackmussii B13, and an experimental model for a widely distributed group of elements in Proteobacteria. ICEclc is transferred from specialized transfer competent cells, which arise at a frequency of 3-5% in a population at stationary phase. Very little is known about the different factors that control the transfer frequency of this ICE family. Here we report the discovery of a three-gene operon encoded by ICEclc, which exerts global control on transfer initiation. The operon consists of three consecutive regulatory genes, encoding a TetR-type repressor MfsR, a MarR-type regulator and a LysR-type activator TciR. We show that MfsR autoregulates expression of the operon, whereas TciR is a global activator of ICEclc gene expression, but no clear role was yet found for MarR. Deletion of mfsR increases expression of tciR and marR, causing the proportion of transfer competent cells to reach almost 100% and transfer frequencies to approach 1 per donor. mfsR deletion also caused a two orders of magnitude loss in population viability, individual cell growth arrest and loss of ICEclc. This indicates that autoregulation is an important feature maintaining ICE transfer but avoiding fitness loss. Bioinformatic analysis showed that the mfsR-marR-tciR operon is unique for ICEclc and a few highly related ICE, whereas tciR orthologues occur more widely in a large variety of suspected ICE among Proteobacteria.
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spelling pubmed-40637392014-06-25 An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13 Pradervand, Nicolas Sulser, Sandra Delavat, François Miyazaki, Ryo Lamas, Iker van der Meer, Jan Roelof PLoS Genet Research Article The integrative and conjugative element ICEclc is a mobile genetic element in Pseudomonas knackmussii B13, and an experimental model for a widely distributed group of elements in Proteobacteria. ICEclc is transferred from specialized transfer competent cells, which arise at a frequency of 3-5% in a population at stationary phase. Very little is known about the different factors that control the transfer frequency of this ICE family. Here we report the discovery of a three-gene operon encoded by ICEclc, which exerts global control on transfer initiation. The operon consists of three consecutive regulatory genes, encoding a TetR-type repressor MfsR, a MarR-type regulator and a LysR-type activator TciR. We show that MfsR autoregulates expression of the operon, whereas TciR is a global activator of ICEclc gene expression, but no clear role was yet found for MarR. Deletion of mfsR increases expression of tciR and marR, causing the proportion of transfer competent cells to reach almost 100% and transfer frequencies to approach 1 per donor. mfsR deletion also caused a two orders of magnitude loss in population viability, individual cell growth arrest and loss of ICEclc. This indicates that autoregulation is an important feature maintaining ICE transfer but avoiding fitness loss. Bioinformatic analysis showed that the mfsR-marR-tciR operon is unique for ICEclc and a few highly related ICE, whereas tciR orthologues occur more widely in a large variety of suspected ICE among Proteobacteria. Public Library of Science 2014-06-19 /pmc/articles/PMC4063739/ /pubmed/24945944 http://dx.doi.org/10.1371/journal.pgen.1004441 Text en © 2014 Pradervand et al http://creativecommons.org/licenses/by/4.0/ 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 properly credited.
spellingShingle Research Article
Pradervand, Nicolas
Sulser, Sandra
Delavat, François
Miyazaki, Ryo
Lamas, Iker
van der Meer, Jan Roelof
An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13
title An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13
title_full An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13
title_fullStr An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13
title_full_unstemmed An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13
title_short An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICEclc in Pseudomonas knackmussii B13
title_sort operon of three transcriptional regulators controls horizontal gene transfer of the integrative and conjugative element iceclc in pseudomonas knackmussii b13
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063739/
https://www.ncbi.nlm.nih.gov/pubmed/24945944
http://dx.doi.org/10.1371/journal.pgen.1004441
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