Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes

Abstract Background The human pathogen Streptococcus pyogenes, or group A Streptococcus, is responsible for mild infections to life-threatening diseases. To facilitate the characterization of regulatory networks involved in the adaptation of this pathogen to its different environments and their evol...

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Main Authors: Isabelle Rosinski-Chupin, Elisabeth Sauvage, Agnès Fouet, Claire Poyart, Philippe Glaser
Format: Article
Language:English
Published: BMC 2019-03-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5613-5
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spelling doaj-76d6204615924ab2947a22329a9388d72020-11-25T03:29:40ZengBMCBMC Genomics1471-21642019-03-0120111510.1186/s12864-019-5613-5Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapesIsabelle Rosinski-Chupin0Elisabeth Sauvage1Agnès Fouet2Claire Poyart3Philippe Glaser4Ecology and Evolution of Resistance to Antibiotics, Institut Pasteur-APHP-Université Paris Saclay, UMR3525 CNRSEcology and Evolution of Resistance to Antibiotics, Institut Pasteur-APHP-Université Paris Saclay, UMR3525 CNRSINSERM U1016, Institut Cochin, CNRS UMR 8104, Université Paris Descartes (UMR-S1016)INSERM U1016, Institut Cochin, CNRS UMR 8104, Université Paris Descartes (UMR-S1016)Ecology and Evolution of Resistance to Antibiotics, Institut Pasteur-APHP-Université Paris Saclay, UMR3525 CNRSAbstract Background The human pathogen Streptococcus pyogenes, or group A Streptococcus, is responsible for mild infections to life-threatening diseases. To facilitate the characterization of regulatory networks involved in the adaptation of this pathogen to its different environments and their evolution, we have determined the primary transcriptome of a serotype M1 S. pyogenes strain at single-nucleotide resolution and compared it with that of Streptococcus agalactiae, also from the pyogenic group of streptococci. Results By using a combination of differential RNA-sequencing and oriented RNA-sequencing we have identified 892 transcription start sites (TSS) and 885 promoters in the S. pyogenes M1 strain S119. 8.6% of S. pyogenes mRNAs were leaderless, among which 81% were also classified as leaderless in S. agalactiae. 26% of S. pyogenes transcript 5′ untranslated regions (UTRs) were longer than 60 nt. Conservation of long 5′ UTRs with S. agalactiae allowed us to predict new potential regulatory sequences. In addition, based on the mapping of 643 transcript ends in the S. pyogenes strain S119, we constructed an operon map of 401 monocistrons and 349 operons covering 81.5% of the genome. One hundred fifty-six operons and 254 monocistrons retained the same organization, despite multiple genomic reorganizations between S. pyogenes and S. agalactiae. Genomic reorganization was found to more often go along with variable promoter sequences and 5′ UTR lengths. Finally, we identified 117 putative regulatory RNAs, among which nine were regulated in response to magnesium concentration. Conclusions Our data provide insights into transcriptome evolution in pyogenic streptococci and will facilitate the analysis of genetic polymorphisms identified by comparative genomics in S. pyogenes.http://link.springer.com/article/10.1186/s12864-019-5613-5Regulatory RNAs5′ UTRsPromotersOperonsRegulatory network evolutionAntisense transcription
collection DOAJ
language English
format Article
sources DOAJ
author Isabelle Rosinski-Chupin
Elisabeth Sauvage
Agnès Fouet
Claire Poyart
Philippe Glaser
spellingShingle Isabelle Rosinski-Chupin
Elisabeth Sauvage
Agnès Fouet
Claire Poyart
Philippe Glaser
Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes
BMC Genomics
Regulatory RNAs
5′ UTRs
Promoters
Operons
Regulatory network evolution
Antisense transcription
author_facet Isabelle Rosinski-Chupin
Elisabeth Sauvage
Agnès Fouet
Claire Poyart
Philippe Glaser
author_sort Isabelle Rosinski-Chupin
title Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes
title_short Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes
title_full Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes
title_fullStr Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes
title_full_unstemmed Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes
title_sort conserved and specific features of streptococcus pyogenes and streptococcus agalactiae transcriptional landscapes
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-03-01
description Abstract Background The human pathogen Streptococcus pyogenes, or group A Streptococcus, is responsible for mild infections to life-threatening diseases. To facilitate the characterization of regulatory networks involved in the adaptation of this pathogen to its different environments and their evolution, we have determined the primary transcriptome of a serotype M1 S. pyogenes strain at single-nucleotide resolution and compared it with that of Streptococcus agalactiae, also from the pyogenic group of streptococci. Results By using a combination of differential RNA-sequencing and oriented RNA-sequencing we have identified 892 transcription start sites (TSS) and 885 promoters in the S. pyogenes M1 strain S119. 8.6% of S. pyogenes mRNAs were leaderless, among which 81% were also classified as leaderless in S. agalactiae. 26% of S. pyogenes transcript 5′ untranslated regions (UTRs) were longer than 60 nt. Conservation of long 5′ UTRs with S. agalactiae allowed us to predict new potential regulatory sequences. In addition, based on the mapping of 643 transcript ends in the S. pyogenes strain S119, we constructed an operon map of 401 monocistrons and 349 operons covering 81.5% of the genome. One hundred fifty-six operons and 254 monocistrons retained the same organization, despite multiple genomic reorganizations between S. pyogenes and S. agalactiae. Genomic reorganization was found to more often go along with variable promoter sequences and 5′ UTR lengths. Finally, we identified 117 putative regulatory RNAs, among which nine were regulated in response to magnesium concentration. Conclusions Our data provide insights into transcriptome evolution in pyogenic streptococci and will facilitate the analysis of genetic polymorphisms identified by comparative genomics in S. pyogenes.
topic Regulatory RNAs
5′ UTRs
Promoters
Operons
Regulatory network evolution
Antisense transcription
url http://link.springer.com/article/10.1186/s12864-019-5613-5
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