Divergent Evolution and Local Establishment of Multidrug‐Resistant Shigella sonnei in China

TL;DR

The study traces the evolution of multidrug-resistant Shigella sonnei in China, revealing distinct genetic lineages and resistance mechanisms.

Contribution

The paper identifies divergent evolutionary pathways and plasmid-mediated resistance mechanisms in Chinese Shigella sonnei strains.

Findings

Shigella sonnei in China evolved into four clades, with distinct resistance mechanisms.

CefRaziR in lineage I was mediated by an IncB/O/K/Z plasmid carrying multiple resistance genes.

ONPG-negative variants resulted from a deletion spanning approximately 10 kbp.

Abstract

This study explored the microevolution of Shigella sonnei in China, focusing on 281 isolates exhibiting coresistance to ceftriaxone and azithromycin (cefRaziR) and 99 ONPG‐negative isolates. Phylogenetic analysis revealed that waterborne outbreak strains, characterized by multidrug resistance (MDR) and cefRaziR, clustered within the predominant domestic lineage I. In contrast, sporadic MDR strains harboring a wider array of antimicrobial resistance (AMR) genes were primarily associated with lineage II. The cefRaziR phenotype in lineage I was mediated by an IncB/O/K/Z plasmid carrying bla
CTX‐M‐14, mphA, aac(3)‐IId, dfrA17, aadA5, and sul1 genes. Lineage II strains acquired cefRaziR through a distinct IncFII plasmid possessing bla
CTX‐M‐15, ermB, and mphA genes, and additionally carried a separate IncB/O/K/Z plasmid backbone with bla
TEM‐1, dfrA12, sul2, strA, strB, tet(A), and aac(3)‐IId genes. Conversion to the ONPG‐negative phenotype was linked to a deletion spanning approximately 10 kbp, which included two insertion sequences (IS1 and IS600), the mhpBAR operon, and the lacIZY operon. Genomic comparisons identified 66 SNPs and 9 accessory genes correlated with lineage II, and 23 SNPs with 9 accessory genes associated with ONPG‐negative variants. Ongoing surveillance of S. sonnei epidemic clones is essential to elucidate their microevolution, track transmission, and assess public health implications.

• Evolutionary history and local establishment of Chinese Shigella sonnei are unclear.

• Chinese S. sonnei developed into four clades and ONPG‐negative variants.

• The antimicrobial resistance phenotype of Clade I was due to an IncB/O/K/Z plasmid.

• Antimicrobial resistance of Clade II was due to IncFII and IncB/O/K/Z plasmids.

• The ONPG‐negative phenotype was attributed to the deletion of a nucleotide region.

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