Abstract
Antibiotic-resistant Campylobacter constitutes a serious threat to public health. The clonal expansion of resistant strains and/or the horizontal spread of resistance genes to other strains and species can hinder the clinical effectiveness of antibiotics to treat severe campylobacteriosis. Still, gaps exist in our understanding of the risks of acquisition and spread of antibiotic resistance in Campylobacter. While the in vitro transfer of antimicrobial resistance genes between Campylobacter species via natural transformation has been extensively demonstrated, experimental studies have favored the use of naked DNA to obtain transformants. In this study, we used experimental designs closer to real-world conditions to evaluate the possible transfer of antimicrobial resistance genes between Campylobacter strains of the same or different species (Campylobacter coli or Campylobacter jejuni) and originating from different animal hosts (swine or turkeys). This was evaluated in vitro through co-culture experiments and in vivo with dual-strain inoculation of turkeys, followed by whole genome sequencing of parental and newly emerged strains. In vitro, we observed four independent horizontal gene transfer events leading to the acquisition of resistance to beta-lactams (blaOXA), aminoglycosides [aph(2′′)-If and rpsL] and tetracycline [tet(O)]. Observed events involved the displacement of resistance-associated genes by a mutated version, or the acquisition of genomic islands harboring a resistance determinant by homologous recombination; we did not detect the transfer of resistance-carrying plasmids even though they were present in some strains. In vivo, we recovered a newly emerged strain with dual-resistance pattern and identified the replacement of an existing non-functional tet(O) by a functional tet(O) in the recipient strain. Whole genome comparisons allowed characterization of the events involved in the horizontal spread of resistance genes between Campylobacter following in vitro co-culture and in vivo dual inoculation. Our study also highlights the potential for antimicrobial resistance transfer across Campylobacter species originating from turkeys and swine, which may have implications for farms hosting both species in close proximity.
Highlights
With an estimated 9.4 million yearly cases in the United States alone, human foodborne diseases are an important public health concern (Scallan et al, 2011)
Phenotypic and genotypic resistance patterns of Campylobacter strains used in the co-culture experiments are summarized in Table 3, and minimum inhibitory concentration (MIC) results are provided in Supplementary Table S2
Our analyses identified two genes associated with aminoglycoside resistance in different strains: aph(2′′)-If associated with both kanamycin and gentamicin resistance (Yao et al, 2017), and aph(3′)-IIIa associated with resistance to kanamycin but not to gentamicin (Gibreel et al, 2004; Crespo et al, 2016; Table 3)
Summary
With an estimated 9.4 million yearly cases in the United States alone, human foodborne diseases are an important public health concern (Scallan et al, 2011). While campylobacteriosis is largely a self-limiting illness, it is accompanied by acute gastroenteritis and is a leading antecedent for the severe autoimmune complication Guillain-Barré syndrome (Allos, 1997; Nachamkin, 2002; Scallan Walter et al, 2020). This, together with additional autoimmune sequelae, such as post-infectious irritable bowel syndrome and reactive arthritis, confers a high disease burden to human campylobacteriosis in the United States and worldwide (Batz et al, 2013; Kirk et al, 2015; Scallan et al, 2015; Scallan Walter et al, 2019). Poultry are recognized as the most important animal reservoir for infection to humans, with 60–80% of human cases in Europe attributable to exposure to raw or undercooked poultry products [European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC), 2015]
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