Shared antibiotic resistance and virulence genes in Staphylococcus aureus from diverse animal hosts

Abstract

The emergence of methicillin-resistant Staphylococcus aureus (MRSA) poses an important threat in human and animal health. In this study, we ask whether resistance and virulence genes in S. aureus are homogeneously distributed or constrained by different animal hosts. We carried out whole genome sequencing of 114 S. aureus isolates from ten species of animals sampled from four New England states (USA) in 2017-2019. The majority of the isolates came from cats, cows and dogs. The maximum likelihood phylogenetic tree based on the alignment of 89,143 single nucleotide polymorphisms of 1173 core genes reveal 31 sequence types (STs). The most common STs were ST5, ST8, ST30, ST133 and ST2187. Every genome carried at least eight acquired resistance genes. Genes related to resistance found in all genomes included norA (fluoroquinolone), arlRS (fluoroquinolone), lmrS (multidrug), tet(38) (tetracycline) and mepAR (multidrug and tigecycline resistance). The most common superantigen genes were tsst-1, sea and sec. Acquired antibiotic resistance (n = 10) and superantigen (n = 9) genes of S. aureus were widely shared between S. aureus lineages and between strains from different animal hosts. These analyses provide insights for considering bacterial gene sharing when developing strategies to combat the emergence of high-risk clones in animals.

Figure 1

Phylogenetic diversity and sources of animal-associated S. aureus in New England. (A) Midpoint-rooted maximum likelihood phylogenetic tree. Tree scale represent the number of substitutions per site. For visual clarity, only those STs with at least three isolates are labeled. (B) Geographical distribution of STs. Pie charts show the proportion of major STs shown in panel A. Light gray includes STs consisting of a single isolate and novel STs, while dark gray represents STs consisting of two isolates. The number in parentheses indicates the number of isolates from each state. Maps were created using QGIS v3.22 (https://www.qgis.org/en/site/) (C) Number of isolates from different animal hosts.

Figure 2

Antibiotic resistance profiles of animal-associated S. aureus in New England. (A) Distribution of acquired antibiotic resistance genes. The genes are color-coded according to resistance mechanisms. The type of SCCmec is also shown. Asterisks indicate genes associated with antibiotic resistance regulation. (B) Number of antibiotic resistance genes per genome. (C) Comparison of number of resistance genes per S. aureus genome in cats, cows and dogs. Significance was estimated using Welch’s t-test.

Figure 3

Virulence profiles of animal-associated S. aureus in New England. (A) Phylogenetic distribution of superantigen genes (shown in presence [red] or absence [white] matrix) and total number of virulence genes (shown in bar plots). (B) Number of virulence genes per S. aureus genome in cats, cows and dogs. (C) Number of superantigen genes per S. aureus genome in cats, cows and dogs. Significance was estimated using Welch’s t-test.

Figure 4

Distribution of antibiotic resistance (A) and superantigen (B) genes in S. aureus from cats, cows, and dogs. Only genes present in more than one isolate are shown and only the three most common animals were included. The outer ring of the upper half of circos plots represent the number of isolates sampled from dogs (purple), cows (light blue), and cats (light green). The outer ring of the bottom half of the circos plots represent the number of isolates that carry the shared antibiotic resistance genes (panel A) and superantigen genes (panel B). Connecting lines between the specific gene and the animal host are shown if the gene was detected in isolates from any of the three animal hosts.