Dataset Information

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 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.

SUBMITTER: Rosinski-Chupin I

PROVIDER: S-EPMC6431027 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Three vancomycin-resistant streptococcal strains carrying vanG elements (two invasive Streptococcus agalactiae isolates [GBS-NY and GBS-NM, both serotype II and multilocus sequence type 22] and one Streptococcus anginosus [Sa]) were examined. The 45,585-bp elements found within Sa and GBS-NY were nearly identical (together designated vanG-1) and shared near-identity over an ~15-kb overlap with a previously described vanG element from Enterococcus faecalis. Unexpectedly, vanG-1 shared much less homology with the 49,321-bp vanG-2 element from GBS-NM, with widely different levels (50% to 99%) of sequence identity shared among 44 related open reading frames. Immediately adjacent to both vanG-1 and vanG-2 were 44,670-bp and 44,680-bp integrative conjugative element (ICE)-like sequences, designated ICE-r, that were nearly identical in the two group B streptococcal (GBS) strains. The dual vanG and ICE-r elements from both GBS strains were inserted at the same position, between bases 1328 and 1329, within the identical RNA methyltransferase (rumA) genes. A GenBank search revealed that although most GBS strains contained insertions within this specific site, only sequence type 22 (ST22) GBS strains contained highly related ICE-r derivatives. The vanG-1 element in Sa was also inserted within this position corresponding to its rumA homolog adjacent to an ICE-r derivative. vanG-1 insertions were previously reported within the same relative position in the E. faecalis rumA homolog. An ICE-r sequence perfectly conserved with respect to its counterpart in GBS-NY was apparent within the same site of the rumA homolog of a Streptococcus dysgalactiae subsp. equisimilis strain. Additionally, homologous vanG-like elements within the conserved rumA target site were evident in Roseburia intestinalis. Importance: These three streptococcal strains represent the first known vancomycin-resistant strains of their species. The collective observations made from these strains reveal a specific hot spot for insertional elements that is conserved between streptococci and different Gram-positive species. The two GBS strains potentially represent a GBS lineage that is predisposed to insertion of vanG elements.