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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)
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.
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.
Silencing of bacterial competence
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