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Research Article

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

Laetitia Attaiech, Aïda Boughammoura, Céline Brochier-Armanet, Omran Allatif, Flora Peillard-Fiorente, Ross A. Edwards, Ayat R. Omar, Andrew M. MacMillan, Mark Glover, and Xavier Charpentier
PNAS first published July 18, 2016; https://doi.org/10.1073/pnas.1601626113
Laetitia Attaiech
aCNRS UMR5240, Microbiologie Adaptation et Pathogénie, 69622 Villeurbanne, France;
bUniversité Claude Bernard Lyon 1, 69100 Villeurbanne, France;
cInternational Center for Infectiology Research (CIRI), International Center for Infectiology Research, Université de Lyon, 69364 Lyon, France;
dINSERM U1111, 69364 Lyon, France;
eEcole Normale Supérieure de Lyon, 69364 Lyon, France;
fUniversité Claude Bernard Lyon 1, Centre International de Recherche en Infectiologie, 69364 Lyon, France;
gCNRS UMR5308, 69007 Lyon, France;
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Aïda Boughammoura
aCNRS UMR5240, Microbiologie Adaptation et Pathogénie, 69622 Villeurbanne, France;
bUniversité Claude Bernard Lyon 1, 69100 Villeurbanne, France;
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Céline Brochier-Armanet
hLaboratoire de Biométrie et Biologie Evolutive, CNRS UMR5558, Université de Lyon, Université Lyon 1, F-69622 Villeurbanne, France;
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Omran Allatif
cInternational Center for Infectiology Research (CIRI), International Center for Infectiology Research, Université de Lyon, 69364 Lyon, France;
dINSERM U1111, 69364 Lyon, France;
eEcole Normale Supérieure de Lyon, 69364 Lyon, France;
fUniversité Claude Bernard Lyon 1, Centre International de Recherche en Infectiologie, 69364 Lyon, France;
gCNRS UMR5308, 69007 Lyon, France;
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Flora Peillard-Fiorente
aCNRS UMR5240, Microbiologie Adaptation et Pathogénie, 69622 Villeurbanne, France;
bUniversité Claude Bernard Lyon 1, 69100 Villeurbanne, France;
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Ross A. Edwards
iDepartment of Biochemistry, University of Alberta, Edmonton, AB T6G 2H7, Canada
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Ayat R. Omar
iDepartment of Biochemistry, University of Alberta, Edmonton, AB T6G 2H7, Canada
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Andrew M. MacMillan
iDepartment of Biochemistry, University of Alberta, Edmonton, AB T6G 2H7, Canada
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Mark Glover
iDepartment of Biochemistry, University of Alberta, Edmonton, AB T6G 2H7, Canada
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Xavier Charpentier
aCNRS UMR5240, Microbiologie Adaptation et Pathogénie, 69622 Villeurbanne, France;
bUniversité Claude Bernard Lyon 1, 69100 Villeurbanne, France;
cInternational Center for Infectiology Research (CIRI), International Center for Infectiology Research, Université de Lyon, 69364 Lyon, France;
dINSERM U1111, 69364 Lyon, France;
eEcole Normale Supérieure de Lyon, 69364 Lyon, France;
fUniversité Claude Bernard Lyon 1, Centre International de Recherche en Infectiologie, 69364 Lyon, France;
gCNRS UMR5308, 69007 Lyon, France;
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  • For correspondence: xavier.charpentier@univ-lyon1.fr
  1. Edited by Ralph R. Isberg, Howard Hughes Medical Institute/Tufts University School of Medicine, Boston, MA, and approved May 26, 2016 (received for review January 29, 2016)

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Significance

Natural transformation is a major mechanism of horizontal gene transfer (HGT) by which bacteria take up exogenous DNA directly in their environment and integrate it in their genome. Acquiring new genetic information may confer an adaptive advantage but an uncontrolled uptake of foreign DNA may be harmful. We document a previously unsuspected means to control HGT by natural transformation in the human pathogen Legionella pneumophila. We found that the DNA uptake system required for natural transformation is subjected to silencing. A member of the widespread ProQ/FinO domain-containing protein family acts as an RNA chaperone and allows the targeting of the mRNAs of the genes coding the DNA uptake system by a newly identified trans-acting small RNA.

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.

  • natural transformation
  • RNA chaperone
  • non-coding RNA
  • Legionella pneumophila
  • ProQ/FinO

Footnotes

  • ↵1To whom correspondence should be addressed. Email: xavier.charpentier{at}univ-lyon1.fr.
  • Author contributions: L.A., A.B., C.B.-A., A.M.M., M.G., and X.C. designed research; L.A., A.B., C.B.-A., F.P.-F., R.A.E., A.R.O., and X.C. performed research; O.A. contributed new reagents/analytic tools; O.A. performed statistical analyses; L.A., A.B., C.B.-A., R.A.E., A.R.O., A.M.M., M.G., and X.C. analyzed data; and L.A., C.B.-A., M.G., and X.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: RNA-seq data were deposited to the MINSEQE-compliant public ArrayExpress database, https://www.ebi.ac.uk/arrayexpress (accession no. E-MTAB-4094) and brokered to the European Nucleotide Archive, www.ebi.ac.uk (accession no. ERP013398).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1601626113/-/DCSupplemental.

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Silencing of bacterial competence
Laetitia Attaiech, Aïda Boughammoura, Céline Brochier-Armanet, Omran Allatif, Flora Peillard-Fiorente, Ross A. Edwards, Ayat R. Omar, Andrew M. MacMillan, Mark Glover, Xavier Charpentier
Proceedings of the National Academy of Sciences Jul 2016, 201601626; DOI: 10.1073/pnas.1601626113

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Silencing of bacterial competence
Laetitia Attaiech, Aïda Boughammoura, Céline Brochier-Armanet, Omran Allatif, Flora Peillard-Fiorente, Ross A. Edwards, Ayat R. Omar, Andrew M. MacMillan, Mark Glover, Xavier Charpentier
Proceedings of the National Academy of Sciences Jul 2016, 201601626; DOI: 10.1073/pnas.1601626113
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