Literature DB >> 27432973

Silencing of natural transformation by an RNA chaperone and a multitarget small RNA.

Laetitia Attaiech1, Aïda Boughammoura2, Céline Brochier-Armanet3, Omran Allatif4, Flora Peillard-Fiorente2, Ross A Edwards5, Ayat R Omar5, Andrew M MacMillan5, Mark Glover5, Xavier Charpentier6.   

Abstract

A highly conserved DNA uptake system allows many bacteria to actively import and integrate exogenous DNA. This process, called natural transformation, represents a major mechanism of horizontal gene transfer (HGT) involved in the acquisition of virulence and antibiotic resistance determinants. Despite evidence of HGT and the high level of conservation of the genes coding the DNA uptake system, most bacterial species appear non-transformable under laboratory conditions. In naturally transformable species, the DNA uptake system is only expressed when bacteria enter a physiological state called competence, which develops under specific conditions. Here, we investigated the mechanism that controls expression of the DNA uptake system in the human pathogen Legionella pneumophila We found that a repressor of this system displays a conserved ProQ/FinO domain and interacts with a newly characterized trans-acting sRNA, RocR. Together, they target mRNAs of the genes coding the DNA uptake system to control natural transformation. This RNA-based silencing represents a previously unknown regulatory means to control this major mechanism of HGT. Importantly, these findings also show that chromosome-encoded ProQ/FinO domain-containing proteins can assist trans-acting sRNAs and that this class of RNA chaperones could play key roles in post-transcriptional gene regulation throughout bacterial species.

Entities:  

Keywords:  Legionella pneumophila; ProQ/FinO; RNA chaperone; natural transformation; non-coding RNA

Mesh:

Substances:

Year:  2016        PMID: 27432973      PMCID: PMC4978251          DOI: 10.1073/pnas.1601626113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  44 in total

1.  Loss of RNase R induces competence development in Legionella pneumophila.

Authors:  Xavier Charpentier; Sébastien P Faucher; Sergey Kalachikov; Howard A Shuman
Journal:  J Bacteriol       Date:  2008-10-10       Impact factor: 3.490

2.  ComEA is a DNA receptor for transformation of competent Bacillus subtilis.

Authors:  R Provvedi; D Dubnau
Journal:  Mol Microbiol       Date:  1999-01       Impact factor: 3.501

3.  FastTree 2--approximately maximum-likelihood trees for large alignments.

Authors:  Morgan N Price; Paramvir S Dehal; Adam P Arkin
Journal:  PLoS One       Date:  2010-03-10       Impact factor: 3.240

Review 4.  Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental Gram-negative bacteria.

Authors:  Patrick Seitz; Melanie Blokesch
Journal:  FEMS Microbiol Rev       Date:  2012-09-20       Impact factor: 16.408

5.  Induction of competence for natural transformation in Legionella pneumophila and exploitation for mutant construction.

Authors:  Carmen Buchrieser; Xavier Charpentier
Journal:  Methods Mol Biol       Date:  2013

6.  The Legionella pneumophila orphan sensor kinase LqsT regulates competence and pathogen-host interactions as a component of the LAI-1 circuit.

Authors:  Aline Kessler; Ursula Schell; Tobias Sahr; André Tiaden; Christopher Harrison; Carmen Buchrieser; Hubert Hilbi
Journal:  Environ Microbiol       Date:  2012-10-04       Impact factor: 5.491

7.  MAFFT multiple sequence alignment software version 7: improvements in performance and usability.

Authors:  Kazutaka Katoh; Daron M Standley
Journal:  Mol Biol Evol       Date:  2013-01-16       Impact factor: 16.240

8.  A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA.

Authors:  Isabelle Mortier-Barrière; Marion Velten; Pauline Dupaigne; Nicolas Mirouze; Olivier Piétrement; Stephen McGovern; Gwennaele Fichant; Bernard Martin; Philippe Noirot; Eric Le Cam; Patrice Polard; Jean-Pierre Claverys
Journal:  Cell       Date:  2007-09-07       Impact factor: 41.582

9.  Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity.

Authors:  Christel Cazalet; Christophe Rusniok; Holger Brüggemann; Nora Zidane; Arnaud Magnier; Laurence Ma; Magalie Tichit; Sophie Jarraud; Christiane Bouchier; François Vandenesch; Frank Kunst; Jérôme Etienne; Philippe Glaser; Carmen Buchrieser
Journal:  Nat Genet       Date:  2004-10-03       Impact factor: 38.330

10.  voom: Precision weights unlock linear model analysis tools for RNA-seq read counts.

Authors:  Charity W Law; Yunshun Chen; Wei Shi; Gordon K Smyth
Journal:  Genome Biol       Date:  2014-02-03       Impact factor: 13.583

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  33 in total

1.  A ProQ/FinO family protein involved in plasmid copy number control favours fitness of bacteria carrying mcr-1-bearing IncI2 plasmids.

Authors:  Jun Yang; Hai-Hong Wang; Yaoyao Lu; Ling-Xian Yi; Yinyue Deng; Luchao Lv; Vincent Burrus; Jian-Hua Liu
Journal:  Nucleic Acids Res       Date:  2021-04-19       Impact factor: 16.971

2.  Bacterial genetics: A new class of Hfq-like sRNA chaperones?

Authors:  Naomi Attar
Journal:  Nat Rev Microbiol       Date:  2016-07-25       Impact factor: 60.633

Review 3.  Silently transformable: the many ways bacteria conceal their built-in capacity of genetic exchange.

Authors:  Laetitia Attaiech; Xavier Charpentier
Journal:  Curr Genet       Date:  2016-11-08       Impact factor: 3.886

4.  GRIL-seq provides a method for identifying direct targets of bacterial small regulatory RNA by in vivo proximity ligation.

Authors:  Kook Han; Brian Tjaden; Stephen Lory
Journal:  Nat Microbiol       Date:  2016-12-22       Impact factor: 17.745

Review 5.  Small Alarmone Synthetases as novel bacterial RNA-binding proteins.

Authors:  Vasili Hauryliuk; Gemma C Atkinson
Journal:  RNA Biol       Date:  2017-10-03       Impact factor: 4.652

Review 6.  ProQ/FinO-domain proteins: another ubiquitous family of RNA matchmakers?

Authors:  Mikolaj Olejniczak; Gisela Storz
Journal:  Mol Microbiol       Date:  2017-05-03       Impact factor: 3.501

7.  Grad-seq guides the discovery of ProQ as a major small RNA-binding protein.

Authors:  Alexandre Smirnov; Konrad U Förstner; Erik Holmqvist; Andreas Otto; Regina Günster; Dörte Becher; Richard Reinhardt; Jörg Vogel
Journal:  Proc Natl Acad Sci U S A       Date:  2016-09-26       Impact factor: 11.205

Review 8.  New sequencing methodologies reveal interplay between multiple RNA-binding proteins and their RNAs.

Authors:  Sahar Melamed
Journal:  Curr Genet       Date:  2020-03-19       Impact factor: 3.886

Review 9.  Prevalence of small base-pairing RNAs derived from diverse genomic loci.

Authors:  Philip P Adams; Gisela Storz
Journal:  Biochim Biophys Acta Gene Regul Mech       Date:  2020-03-05       Impact factor: 4.490

10.  Determinants of RNA recognition by the FinO domain of the Escherichia coli ProQ protein.

Authors:  Ewa M Stein; Joanna Kwiatkowska; Maciej M Basczok; Chandra M Gravel; Katherine E Berry; Mikołaj Olejniczak
Journal:  Nucleic Acids Res       Date:  2020-07-27       Impact factor: 16.971

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