Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer

Streptococcus agalactiae or Group B Streptococcus (GBS) are opportunistic bacteria that can cause lethal sepsis in children and immuno-compromised patients. Their genome is a reservoir of mobile genetic elements that can be horizontally transferred. Among them, integrative and conjugative elements (...

Full description

Bibliographic Details
Main Authors: Fabian Lorenzo-Diaz, Cris Fernández-Lopez, Pierre-Emmanuel Douarre, Adrian Baez-Ortega, Carlos Flores, Philippe Glaser, Manuel Espinosa
Format: Article
Language:English
Published: The Royal Society 2016-01-01
Series:Open Biology
Subjects:
Online Access:https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.160084
_version_ 1818939035500937216
author Fabian Lorenzo-Diaz
Cris Fernández-Lopez
Pierre-Emmanuel Douarre
Adrian Baez-Ortega
Carlos Flores
Philippe Glaser
Manuel Espinosa
author_facet Fabian Lorenzo-Diaz
Cris Fernández-Lopez
Pierre-Emmanuel Douarre
Adrian Baez-Ortega
Carlos Flores
Philippe Glaser
Manuel Espinosa
author_sort Fabian Lorenzo-Diaz
collection DOAJ
description Streptococcus agalactiae or Group B Streptococcus (GBS) are opportunistic bacteria that can cause lethal sepsis in children and immuno-compromised patients. Their genome is a reservoir of mobile genetic elements that can be horizontally transferred. Among them, integrative and conjugative elements (ICEs) and the smaller integrative and mobilizable elements (IMEs) primarily reside in the bacterial chromosome, yet have the ability to be transferred between cells by conjugation. ICEs and IMEs are therefore a source of genetic variability that participates in the spread of antibiotic resistance. Although IMEs seem to be the most prevalent class of elements transferable by conjugation, they are poorly known. Here, we have studied a GBS-IME, termed IMESag-rpsI, which is widely distributed in GBS despite not carrying any apparent virulence trait. Analyses of 240 whole genomes showed that IMESag-rpsI is present in approximately 47% of the genomes, has a roughly constant size (approx. 9 kb) and is always integrated at a single location, the 3′-end of the gene encoding the ribosomal protein S9 (rpsI). Based on their genetic variation, several IMESag-rpsI types were defined (A–J) and classified in clonal complexes (CCs). CC1 was the most populated by IMESag-rpsI (more than 95%), mostly of type-A (71%). One CC1 strain (S. agalactiae HRC) was deep-sequenced to understand the rationale underlying type-A IMESag-rpsI enrichment in GBS. Thirteen open reading frames were identified, one of them encoding a protein (MobSag) belonging to the broadly distributed family of relaxases MOBV1. Protein MobSag was purified and, by a newly developed method, shown to cleave DNA at a specific dinucleotide. The S. agalactiae HRC-IMESag-rpsI is able to excise from the chromosome, as shown by the presence of circular intermediates, and it harbours a fully functional mobilization module. Further, the mobSag gene encoded by this mobile element is able to promote plasmid transfer among pneumococcal strains, suggesting that MobSag facilitates the spread of IMESag-rpsI and that this spread would explain the presence of the same IMESag-rpsI type in GBS strains belonging to different CCs.
first_indexed 2024-12-20T06:17:21Z
format Article
id doaj.art-50469300873f4fa193649314daff8494
institution Directory Open Access Journal
issn 2046-2441
language English
last_indexed 2024-12-20T06:17:21Z
publishDate 2016-01-01
publisher The Royal Society
record_format Article
series Open Biology
spelling doaj.art-50469300873f4fa193649314daff84942022-12-21T19:50:30ZengThe Royal SocietyOpen Biology2046-24412016-01-0161010.1098/rsob.160084160084Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transferFabian Lorenzo-DiazCris Fernández-LopezPierre-Emmanuel DouarreAdrian Baez-OrtegaCarlos FloresPhilippe GlaserManuel EspinosaStreptococcus agalactiae or Group B Streptococcus (GBS) are opportunistic bacteria that can cause lethal sepsis in children and immuno-compromised patients. Their genome is a reservoir of mobile genetic elements that can be horizontally transferred. Among them, integrative and conjugative elements (ICEs) and the smaller integrative and mobilizable elements (IMEs) primarily reside in the bacterial chromosome, yet have the ability to be transferred between cells by conjugation. ICEs and IMEs are therefore a source of genetic variability that participates in the spread of antibiotic resistance. Although IMEs seem to be the most prevalent class of elements transferable by conjugation, they are poorly known. Here, we have studied a GBS-IME, termed IMESag-rpsI, which is widely distributed in GBS despite not carrying any apparent virulence trait. Analyses of 240 whole genomes showed that IMESag-rpsI is present in approximately 47% of the genomes, has a roughly constant size (approx. 9 kb) and is always integrated at a single location, the 3′-end of the gene encoding the ribosomal protein S9 (rpsI). Based on their genetic variation, several IMESag-rpsI types were defined (A–J) and classified in clonal complexes (CCs). CC1 was the most populated by IMESag-rpsI (more than 95%), mostly of type-A (71%). One CC1 strain (S. agalactiae HRC) was deep-sequenced to understand the rationale underlying type-A IMESag-rpsI enrichment in GBS. Thirteen open reading frames were identified, one of them encoding a protein (MobSag) belonging to the broadly distributed family of relaxases MOBV1. Protein MobSag was purified and, by a newly developed method, shown to cleave DNA at a specific dinucleotide. The S. agalactiae HRC-IMESag-rpsI is able to excise from the chromosome, as shown by the presence of circular intermediates, and it harbours a fully functional mobilization module. Further, the mobSag gene encoded by this mobile element is able to promote plasmid transfer among pneumococcal strains, suggesting that MobSag facilitates the spread of IMESag-rpsI and that this spread would explain the presence of the same IMESag-rpsI type in GBS strains belonging to different CCs.https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.160084conjugationhorizontal gene transferintegrative and mobilizable elements mobilizationrelaxasesstreptococcus
spellingShingle Fabian Lorenzo-Diaz
Cris Fernández-Lopez
Pierre-Emmanuel Douarre
Adrian Baez-Ortega
Carlos Flores
Philippe Glaser
Manuel Espinosa
Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer
Open Biology
conjugation
horizontal gene transfer
integrative and mobilizable elements mobilization
relaxases
streptococcus
title Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer
title_full Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer
title_fullStr Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer
title_full_unstemmed Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer
title_short Streptococcal group B integrative and mobilizable element IMESag-rpsI encodes a functional relaxase involved in its transfer
title_sort streptococcal group b integrative and mobilizable element imesag rpsi encodes a functional relaxase involved in its transfer
topic conjugation
horizontal gene transfer
integrative and mobilizable elements mobilization
relaxases
streptococcus
url https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.160084
work_keys_str_mv AT fabianlorenzodiaz streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer
AT crisfernandezlopez streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer
AT pierreemmanueldouarre streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer
AT adrianbaezortega streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer
AT carlosflores streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer
AT philippeglaser streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer
AT manuelespinosa streptococcalgroupbintegrativeandmobilizableelementimesagrpsiencodesafunctionalrelaxaseinvolvedinitstransfer