Abstract
Livestock represent a possible reservoir for facilitating the transmission of the zoonotic foodborne pathogen Salmonella enterica to humans; there is also concern that strains can acquire resistance to antimicrobials in the farm environment. Here, whole-genome sequencing (WGS) was used to characterize Salmonella strains (n = 128) isolated from healthy dairy cattle and their associated environments on 13 New York State farms to assess the diversity and microevolution of this important pathogen at the level of the individual herd. Additionally, the accuracy and concordance of multiple in silico tools are assessed, including: (i) two in silico serotyping tools, (ii) combinations of five antimicrobial resistance (AMR) determinant detection tools and one to five AMR determinant databases, and (iii) one antimicrobial minimum inhibitory concentration (MIC) prediction tool. For the isolates sequenced here, in silico serotyping methods outperformed traditional serotyping and resolved all un-typable and/or ambiguous serotype assignments. Serotypes assigned in silico showed greater congruency with the Salmonella whole-genome phylogeny than traditional serotype assignments, and in silico methods showed high concordance (99% agreement). In silico AMR determinant detection methods additionally showed a high degree of concordance, regardless of the pipeline or database used (≥98% agreement among susceptible/resistant assignments for all pipeline/database combinations). For AMR detection methods that relied exclusively on nucleotide BLAST, accuracy could be maximized by using a range of minimum nucleotide identity and coverage thresholds, with thresholds of 75% nucleotide identity and 50–60% coverage adequate for most pipeline/database combinations. In silico characterization of the microevolution and AMR dynamics of each of six serotype groups (S. Anatum, Cerro, Kentucky, Meleagridis, Newport, Typhimurium/Typhimurium variant Copenhagen) revealed that some lineages were strongly associated with individual farms, while others were distributed across multiple farms. Numerous AMR determinant acquisition and loss events were identified, including the recent acquisition of cephalosporin resistance-conferring blaCMY- and blaCTX–M-type beta-lactamases. The results presented here provide high-resolution insight into the temporal dynamics of AMR Salmonella at the scale of the individual farm and highlight both the strengths and limitations of WGS in tracking zoonotic pathogens and their associated AMR determinants at the livestock-human interface.
Highlights
The foodborne pathogen Salmonella enterica is estimated to be responsible for 1.35 million infections, 26,500 hospitalizations, and 420 deaths each year in the United States alone (Centers for Disease Control and Prevention, 2021)
In silico serotypes assigned using (i) Salmonella in silico Typing Resource (SISTR)’s core-genome multilocus sequence typing approach and (ii) SeqSero2 were both highly congruent with the Salmonella whole-genome phylogeny (Figure 1) and highly concordant with each other: 127 of 128 (99.2%) Salmonella isolates sequenced in this study were assigned to identical in silico serotypes using both SISTR cgMLST and SeqSero2 (Supplementary Table 1), with 100% concordance observed for six of seven observed in silico serotype groups
Cattle may act as a reservoir for Salmonella and may facilitate its transmission to other animals (Mentaberre et al, 2013; Wiethoelter et al, 2015) or humans, either through direct contact or via the food supply chain (Hoelzer et al, 2011; Cummings et al, 2012; Mughini-Gras et al, 2014; An et al, 2017; Gutema et al, 2019)
Summary
The foodborne pathogen Salmonella enterica is estimated to be responsible for 1.35 million infections, 26,500 hospitalizations, and 420 deaths each year in the United States alone (Centers for Disease Control and Prevention, 2021). Despite the fact that over 2,600 Salmonella serotypes have been described (IssenhuthJeanjean et al, 2014), fewer than 100 of these serotypes are responsible for the majority of human infections (Centers for Disease Control and Prevention, 2020). In a previous survey of 46 dairy cattle herds in New York State, Salmonella strains isolated from subclinically infected dairy cattle and associated farm environments spanned 26 serotypes, the most common being Cerro, Kentucky, Typhimurium, Newport, and Anatum (Rodriguez-Rivera et al, 2014). Antimicrobial resistant (AMR) isolates were observed on several farms, on numerous occasions, suggesting subclinically infected dairy cattle as a potential source of AMR Salmonella (Rodriguez-Rivera et al, 2014)
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