Abstract
ABSTRACTMethicillin-susceptible Staphylococcus aureus (MSSA) accounts for the majority of S. aureus infections globally, and yet surprisingly little is known about its clonal evolution. We applied comparative whole-genome sequencing (WGS) analyses to epidemiologically and geographically diverse ST398-MSSA, a pandemic lineage affecting both humans and livestock. Bayesian phylogenetic analysis predicted divergence of human-associated ST398-MSSA ~40 years ago. Isolates from Midwestern pigs and veterinarians differed substantially from those in New York City (NYC). Pig ST398 strains contained a large region of recombination representing imports from multiple sequence types (STs). Phylogeographic analyses supported the spread of ST398-MSSA along local cultural and migratory links between parts of the Caribbean, North America, and France, respectively. Applying pairwise single-nucleotide polymorphism (SNP) distances as a measure of genetic relatedness between isolates, we observed that ST398 not only clustered in households but also frequently extended across local social networks. Isolates collected from environmental surfaces reflected the full diversity of colonizing individuals, highlighting their potentially critical role as reservoirs for transmission and diversification. Strikingly, we observed high within-host SNP variability compared to our previous studies on the dominant methicillin-resistant Staphylococcus aureus (MRSA) clone USA300. Our data indicate that the dynamics of colonization, persistence, and transmission differ substantially between USA300-MRSA and ST398-MSSA. Taken together, our study reveals local and international routes of transmission for a major MSSA clone, indicating key impacts of recombination and mutation on genetic diversification and highlighting important ecological differences from epidemic USA300. Our study demonstrates extensive local and international routes of transmission for a major MSSA clone despite the lack of substantial antibiotic resistance.
Highlights
Methicillin-susceptible Staphylococcus aureus (MSSA) accounts for the majority of S. aureus infections globally, and yet surprisingly little is known about its clonal evolution
IMPORTANCE Unlike methicillin-resistant Staphylococcus aureus (MRSA), surprisingly little is known about the clonal evolution of methicillin-susceptible S. aureus (MSSA), these strains account for the majority of S. aureus infections
In order to determine the evolutionary history of human ST398 MSSA, we determined full-genome sequences of 288 spa-clonal complex (CC) t571/ST398 isolates (Fig. 1; see Table S1 in the supplemental material)
Summary
Methicillin-susceptible Staphylococcus aureus (MSSA) accounts for the majority of S. aureus infections globally, and yet surprisingly little is known about its clonal evolution. The advent of high-resolution whole-genome sequencing (WGS) has allowed the reconstruction of the evolution of several major MRSA clones such as multilocus sequence types (STs) ST239, ST22, ST30, ST80, and ST8/USA300 by sequencing of large data sets [2,3,4,5,6,7] These studies have documented how specific antibiotic selective pressures, as well as interactions with human hosts, have shaped the recent evolutionary history of these MRSA clones. While these studies have included a selected number of methicillin-susceptible S. aureus (MSSA) isolates [7], the emergence, evolution, and transmission of major MSSA lineages have been largely disregarded. MRSA ST398 strains are thought to spread only infrequently beyond the immediate animal and farm contacts [17,18,19]
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