Programmed protection of foreign DNA from restriction allows pathogenicity island exchange during pneumococcal transformation

In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of sexuality, relies on internalized foreign DNA to create genetic diversity, the latter degrade foreign DNA to protect from bacteriophage attack. The huma...

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Published inPLoS pathogens Vol. 9; no. 2; p. e1003178
Main Authors Johnston, Calum, Martin, Bernard, Granadel, Chantal, Polard, Patrice, Claverys, Jean-Pierre
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2013
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Abstract In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of sexuality, relies on internalized foreign DNA to create genetic diversity, the latter degrade foreign DNA to protect from bacteriophage attack. The human pathogen Streptococcus pneumoniae is transformable and possesses either of two R-M systems, DpnI and DpnII, which respectively restrict methylated or unmethylated double-stranded (ds) DNA. S. pneumoniae DpnII strains possess DpnM, which methylates dsDNA to protect it from DpnII restriction, and a second methylase, DpnA, which is induced during competence for genetic transformation and is unusual in that it methylates single-stranded (ss) DNA. DpnA was tentatively ascribed the role of protecting internalized plasmids from DpnII restriction, but this seems unlikely in light of recent results establishing that pneumococcal transformation was not evolved to favor plasmid exchange. Here we validate an alternative hypothesis, showing that DpnA plays a crucial role in the protection of internalized foreign DNA, enabling exchange of pathogenicity islands and more generally of variable regions between pneumococcal isolates. We show that transformation of a 21.7 kb heterologous region is reduced by more than 4 logs in dpnA mutant cells and provide evidence that the specific induction of dpnA during competence is critical for full protection. We suggest that the integration of a restrictase/ssDNA-methylase couplet into the competence regulon maintains protection from bacteriophage attack whilst simultaneously enabling exchange of pathogenicicy islands. This protective role of DpnA is likely to be of particular importance for pneumococcal virulence by allowing free variation of capsule serotype in DpnII strains via integration of DpnI capsule loci, contributing to the documented escape of pneumococci from capsule-based vaccines. Generally, this finding is the first evidence for a mechanism that actively promotes genetic diversity of S. pneumoniae through programmed protection and incorporation of foreign DNA.
AbstractList In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of sexuality, relies on internalized foreign DNA to create genetic diversity, the latter degrade foreign DNA to protect from bacteriophage attack. The human pathogen Streptococcus pneumoniae is transformable and possesses either of two R-M systems, DpnI and DpnII, which respectively restrict methylated or unmethylated double-stranded (ds) DNA. S. pneumoniae DpnII strains possess DpnM, which methylates dsDNA to protect it from DpnII restriction, and a second methylase, DpnA, which is induced during competence for genetic transformation and is unusual in that it methylates single-stranded (ss) DNA. DpnA was tentatively ascribed the role of protecting internalized plasmids from DpnII restriction, but this seems unlikely in light of recent results establishing that pneumococcal transformation was not evolved to favor plasmid exchange. Here we validate an alternative hypothesis, showing that DpnA plays a crucial role in the protection of internalized foreign DNA, enabling exchange of pathogenicity islands and more generally of variable regions between pneumococcal isolates. We show that transformation of a 21.7 kb heterologous region is reduced by more than 4 logs in dpnA mutant cells and provide evidence that the specific induction of dpnA during competence is critical for full protection. We suggest that the integration of a restrictase/ssDNA-methylase couplet into the competence regulon maintains protection from bacteriophage attack whilst simultaneously enabling exchange of pathogenicicy islands. This protective role of DpnA is likely to be of particular importance for pneumococcal virulence by allowing free variation of capsule serotype in DpnII strains via integration of DpnI capsule loci, contributing to the documented escape of pneumococci from capsule-based vaccines. Generally, this finding is the first evidence for a mechanism that actively promotes genetic diversity of S. pneumoniae through programmed protection and incorporation of foreign DNA.
  In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of sexuality, relies on internalized foreign DNA to create genetic diversity, the latter degrade foreign DNA to protect from bacteriophage attack. The human pathogen Streptococcus pneumoniae is transformable and possesses either of two R-M systems, DpnI and DpnII, which respectively restrict methylated or unmethylated double-stranded (ds) DNA. S. pneumoniae DpnII strains possess DpnM, which methylates dsDNA to protect it from DpnII restriction, and a second methylase, DpnA, which is induced during competence for genetic transformation and is unusual in that it methylates single-stranded (ss) DNA. DpnA was tentatively ascribed the role of protecting internalized plasmids from DpnII restriction, but this seems unlikely in light of recent results establishing that pneumococcal transformation was not evolved to favor plasmid exchange. Here we validate an alternative hypothesis, showing that DpnA plays a crucial role in the protection of internalized foreign DNA, enabling exchange of pathogenicity islands and more generally of variable regions between pneumococcal isolates. We show that transformation of a 21.7 kb heterologous region is reduced by more than 4 logs in dpnA mutant cells and provide evidence that the specific induction of dpnA during competence is critical for full protection. We suggest that the integration of a restrictase/ssDNA-methylase couplet into the competence regulon maintains protection from bacteriophage attack whilst simultaneously enabling exchange of pathogenicicy islands. This protective role of DpnA is likely to be of particular importance for pneumococcal virulence by allowing free variation of capsule serotype in DpnII strains via integration of DpnI capsule loci, contributing to the documented escape of pneumococci from capsule-based vaccines. Generally, this finding is the first evidence for a mechanism that actively promotes genetic diversity of S. pneumoniae through programmed protection and incorporation of foreign DNA.
In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of sexuality, relies on internalized foreign DNA to create genetic diversity, the latter degrade foreign DNA to protect from bacteriophage attack. The human pathogen Streptococcus pneumoniae is transformable and possesses either of two R-M systems, DpnI and DpnII, which respectively restrict methylated or unmethylated double-stranded (ds) DNA. S. pneumoniae DpnII strains possess DpnM, which methylates dsDNA to protect it from Dpn II restriction, and a second methylase, DpnA, which is induced during competence for genetic transformation and is unusual in that it methylates single-stranded (ss) DNA. DpnA was tentatively ascribed the role of protecting internalized plasmids from Dpn II restriction, but this seems unlikely in light of recent results establishing that pneumococcal transformation was not evolved to favor plasmid exchange. Here we validate an alternative hypothesis, showing that DpnA plays a crucial role in the protection of internalized foreign DNA, enabling exchange of pathogenicity islands and more generally of variable regions between pneumococcal isolates. We show that transformation of a 21.7 kb heterologous region is reduced by more than 4 logs in dpnA mutant cells and provide evidence that the specific induction of dpnA during competence is critical for full protection. We suggest that the integration of a restrictase/ssDNA-methylase couplet into the competence regulon maintains protection from bacteriophage attack whilst simultaneously enabling exchange of pathogenicicy islands. This protective role of DpnA is likely to be of particular importance for pneumococcal virulence by allowing free variation of capsule serotype in DpnII strains via integration of DpnI capsule loci, contributing to the documented escape of pneumococci from capsule-based vaccines. Generally, this finding is the first evidence for a mechanism that actively promotes genetic diversity of S. pneumoniae through programmed protection and incorporation of foreign DNA. Natural genetic transformation can compensate for the absence of sexual reproduction in bacteria, allowing genetic diversification by recombination. It proceeds through the internalization of single stranded (ss) DNA fragments created from an exogenous double stranded (ds) DNA substrate, which are incorporated into the genome by homology. On the other hand, restriction-modification (R-M) systems, which protect bacteria from bacteriophage attack by degrading invading foreign DNA, potentially antagonize transformation. About half of the strains of the naturally transformable species and human pathogen Streptococcus pneumoniae possess an R-M system, DpnII, restricting unmethylated dsDNA. DpnII strains possess DpnA which is unusual in that it methylates ssDNA. Here we show that DpnA plays a crucial role in the protection of internalized heterologous transforming ssDNA, preventing the post-replicative destruction by DpnII of transformants produced by chromosomal integration of heterogolous DNA by virtue of flanking homology. This protective role of DpnA is of particular importance for acquisition of pathogenicity islands, such as capsule loci, from non-DpnII origin by DpnII strains, likely contributing to pneumococcal virulence via escape from capsule-based vaccines. Generally, this finding is the first evidence for a mechanism that actively promotes genetic diversity of S. pneumoniae through active protection and incorporation of foreign DNA.
Audience Academic
Author Claverys, Jean-Pierre
Polard, Patrice
Granadel, Chantal
Johnston, Calum
Martin, Bernard
AuthorAffiliation Harvard Medical School, United States of America
2 Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, Toulouse, France
1 Centre National de la Recherche Scientifique, LMGM-UMR5100, Toulouse, France
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– name: 2 Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, Toulouse, France
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Johnston et al. 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 credited: Johnston C, Martin B, Granadel C, Polard P, Claverys J-P (2013) Programmed Protection of Foreign DNA from Restriction Allows Pathogenicity Island Exchange during Pneumococcal Transformation. PLoS Pathog 9(2): e1003178. doi:10.1371/journal.ppat.1003178
Distributed under a Creative Commons Attribution 4.0 International License
2013 Johnston et al 2013 Johnston et al
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– notice: 2013 Johnston et al. 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 credited: Johnston C, Martin B, Granadel C, Polard P, Claverys J-P (2013) Programmed Protection of Foreign DNA from Restriction Allows Pathogenicity Island Exchange during Pneumococcal Transformation. PLoS Pathog 9(2): e1003178. doi:10.1371/journal.ppat.1003178
– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: 2013 Johnston et al 2013 Johnston et al
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PMCID: PMC3573125
Conceived and designed the experiments: CJ BM JPC. Performed the experiments: CJ BM CG. Analyzed the data: CJ BM PP JPC. Contributed reagents/materials/analysis tools: CJ CG. Wrote the paper: CJ JPC.
The authors have declared that no competing interests exist.
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SSID ssj0041316
Score 2.3344505
Snippet In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of sexuality,...
  In bacteria, transformation and restriction-modification (R-M) systems play potentially antagonistic roles. While the former, proposed as a form of...
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SourceType Open Website
Open Access Repository
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StartPage e1003178
SubjectTerms Acquisitions & mergers
Bacteria
Bacterial genetics
Biology
Deoxyribonucleases, Type II Site-Specific - genetics
Deoxyribonucleases, Type II Site-Specific - metabolism
DNA
DNA - genetics
DNA Methylation
DNA Transformation Competence - genetics
Efficiency
Genetic aspects
Genetic transformation
Genomes
Genomic Islands - genetics
Health aspects
Humans
Life Sciences
Microbiology
Microbiology and Parasitology
Mutation
Physiological aspects
Plasmids
Plasmids - genetics
Pneumococcal Infections - genetics
Pneumococcal Infections - microbiology
Site-Specific DNA-Methyltransferase (Adenine-Specific) - genetics
Site-Specific DNA-Methyltransferase (Adenine-Specific) - metabolism
Streptococcus infections
Streptococcus pneumoniae
Streptococcus pneumoniae - genetics
Streptococcus pneumoniae - pathogenicity
Vaccines
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Title Programmed protection of foreign DNA from restriction allows pathogenicity island exchange during pneumococcal transformation
URI https://www.ncbi.nlm.nih.gov/pubmed/23459610
https://www.proquest.com/docview/1314344500
https://search.proquest.com/docview/1314893351
https://hal.science/hal-00946761
https://pubmed.ncbi.nlm.nih.gov/PMC3573125
https://doaj.org/article/53d955af0ac74401ba9a5891dce68243
http://dx.doi.org/10.1371/journal.ppat.1003178
Volume 9
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