Genomic insights into the diversity, virulence, and antimicrobial resistance of group B Streptococcus clinical isolates from Saudi Arabia

Front Cell Infect Microbiol. 2024 Apr 22:14:1377993. doi: 10.3389/fcimb.2024.1377993. eCollection 2024.

Abstract

Introduction: Detailed assessment of the population structure of group B Streptococcus (GBS) among adults is still lacking in Saudi Arabia. Here we characterized a representative collection of isolates from colonized and infected adults.

Methods: GBS isolates (n=89) were sequenced by Illumina and screened for virulence and antimicrobial resistance determinants. Genetic diversity was assessed by single nucleotide polymorphisms and core-genome MLST analyses.

Results: Genome sequences revealed 28 sequence types (STs) and nine distinct serotypes, including uncommon serotypes VII and VIII. Majority of these STs (n=76) belonged to the human-associated clonal complexes (CCs) CC1 (33.71%), CC19 (25.84%), CC17 (11.24%), CC10/CC12 (7.87%), and CC452 (6.74%). Major CCs exhibited intra-lineage serotype diversity, except for the hypervirulent CC17, which exclusively expressed serotype III. Virulence profiling revealed that nearly all isolates (94.38%) carried at least one of the four alpha family protein genes (i.e., alphaC, alp1, alp2/3, and rib), and 92.13% expressed one of the two serine-rich repeat surface proteins Srr1 or Srr2. In addition, most isolates harbored the pilus island (PI)-2a alone (15.73%) or in combination with PI-1 (62.92%), and those carrying PI-2b alone (10.11%) belonged to CC17. Phylogenetic analysis grouped the sequenced isolates according to CCs and further subdivided them along with their serotypes. Overall, isolates across all CC1 phylogenetic clusters expressed Srr1 and carried the PI-1 and PI-2a loci, but differed in genes encoding the alpha-like proteins. CC19 clusters were dominated by the III/rib/srr1/PI-1+PI-2a (43.48%, 10/23) and V/alp1/srr1/PI-1+PI-2a (34.78%, 8/23) lineages, whereas most CC17 isolates (90%, 9/10) had the same III/rib/srr2/P1-2b genetic background. Interestingly, genes encoding the CC17-specific adhesins HvgA and Srr2 were detected in phylogenetically distant isolates belonging to ST1212, suggesting that other highly virulent strains might be circulating within the species. Resistance to macrolides and/or lincosamides across all major CCs (n=48) was associated with the acquisition of erm(B) (62.5%, 30/48), erm(A) (27.1%, 13/48), lsa(C) (8.3%, 4/48), and mef(A) (2.1%, 1/48) genes, whereas resistance to tetracycline was mainly mediated by presence of tet(M) (64.18%, 43/67) and tet(O) (20.9%, 14/67) alone or in combination (13.43%, 9/67).

Discussion: These findings underscore the necessity for more rigorous characterization of GBS isolates causing infections.

Keywords: CC17; HvgA; MLST; ST1212; Saudi Arabia; antimicrobial resistance; group B streptococcus; whole-genome sequencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Anti-Bacterial Agents / pharmacology
  • Drug Resistance, Bacterial* / genetics
  • Female
  • Genetic Variation*
  • Genome, Bacterial*
  • Genomics
  • Genotype
  • Humans
  • Microbial Sensitivity Tests
  • Multilocus Sequence Typing*
  • Phylogeny
  • Polymorphism, Single Nucleotide
  • Saudi Arabia
  • Serogroup*
  • Streptococcal Infections* / microbiology
  • Streptococcus agalactiae* / classification
  • Streptococcus agalactiae* / drug effects
  • Streptococcus agalactiae* / genetics
  • Streptococcus agalactiae* / isolation & purification
  • Streptococcus agalactiae* / pathogenicity
  • Virulence / genetics
  • Virulence Factors* / genetics
  • Whole Genome Sequencing

Substances

  • Virulence Factors
  • Anti-Bacterial Agents

Grants and funding

The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.