Genomic epidemiology of Clostridioides difficile sequence type 35 reveals intraspecies and interspecies clonal transmission

Emerg Microbes Infect. 2024 Dec;13(1):2408322. doi: 10.1080/22221751.2024.2408322. Epub 2024 Sep 30.

Abstract

Clostridioides difficile sequence type (ST) 35 has been found in humans and animals worldwide. However, its genomic epidemiology and clonal transmission have not been explored in detail. In this study, 176 C. difficile ST35 isolates from six countries were sequenced. Genomic diversity, clonal transmission and epidemiological data were analyzed. Sporulation and virulence capacities were measured. Four ribotypes (RT) were identified including RT046 (97.2%), RT656 (1.1%), RT427 (0.6%), and RT AI-78 (1.1%). Phylogenetic analysis of 176 ST35 genomes, along with 50 publicly available genomes, revealed two distinctive lineages without time-, region-, or source-dependent distribution. However, the distribution of antimicrobial resistance genes differed significantly between the two lineages. Nosocomial and communal transmission occurred in humans with the isolates differed by ≤ two core-genome single-nucleotide polymorphism (cgSNPs) and clonal circulation was found in pigs with the isolates differed by ≤ four cgSNPs. Notably, interspecies clonal transmission was identified among three patients with community acquired C. difficile infection and pigs with epidemiological links, differed by ≤ nine cgSNPs. Toxin B (TcdB) concentrations were significantly higher in human isolates compared to pig isolates, and ST35 isolates exhibited stronger sporulation capacities than other STs. Our study provided new genomic insights and epidemiological evidence of C. difficile ST35 intraspecies and interspecies clonal transmission, which can also be facilitated by its strong sporulation capacity.

Keywords: Clostridioides difficile; ST35; clonal transmission; genome epidemiology; sporulation capacity; virulence; whole genome sequencing.

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Toxins / genetics
  • Clostridioides difficile* / classification
  • Clostridioides difficile* / genetics
  • Clostridioides difficile* / isolation & purification
  • Clostridium Infections* / epidemiology
  • Clostridium Infections* / microbiology
  • Clostridium Infections* / transmission
  • Cross Infection / epidemiology
  • Cross Infection / microbiology
  • Cross Infection / transmission
  • Drug Resistance, Bacterial / genetics
  • Genome, Bacterial*
  • Genomics
  • Humans
  • Molecular Epidemiology
  • Phylogeny*
  • Polymorphism, Single Nucleotide
  • Ribotyping*
  • Swine
  • Virulence / genetics

Substances

  • Bacterial Proteins
  • Bacterial Toxins

Grants and funding

This work was supported in part by the National Natural Science Foundation of China (82372299), the Key Project of Natural Science Foundation of Zhejiang Province (LXZ22H300001), and the Program for Major Science and Technology Medicine and Healthcare in Zhejiang (WKJ-ZJ-2309).