The Genomic Context for the Evolution and Transmission of Community-Associated Staphylococcus aureus ST59 Through the Food Chain

Abstract

Sequence type 59 (ST59) is a predominant clonal lineage of community-acquired, methicillin-resistant Staphylococcus aureus (CA-MRSA) in Asia. Despite its increasing clinical relevance in China, the evolution and geographic expansion of ST59 has been relatively uncared for. Previous study has shown that ST59 was the predominant clone in food-related MRSA in China. This study compared the genomes of 87 clonal complex (CC) 59 S. aureus isolates sourced from food chain and infection cases to reconstruct the molecular evolution and geographical spread of ST59. Accordingly, three major sub-clades of ST59 were identified and these did not correlate with isolation source or location. Phylogenetic analysis estimated that ST59 in mainland China diverged from a most common recent ancestor around 1974, and most of the cases of cross-country transmission occurred between 1987 and 2000. Notably, two recent events of crosscountry transmission through the food chain were observed, the isolates from these events diverged within relatively short time intervals. These isolates also showed high similarity in terms of their core genome, accessory genes, and antibiotic resistance patterns. These findings provide a valuable insight into the potential route of ST59 expansion in China and indicate a need for robust food chain surveillance to prevent the spread of this pathogen.

Staphylococcus aureus ST59: Concurrent but Separate Evolution of North American and East Asian Lineages

“…Previous studies have suggested that ST59 evolved concurrently in both North America (NA), previously referred to as the United States lineage and East Asia (EA), with strains from each region belonging to separate and distinct sub-lineages ( Ward et al, 2016 ), with mobile genetic elements playing a part ( Hung et al, 2016 ). For a more detailed look into the evolution of the ST59 lineage, a Bayesian inference phylogenomic tree, comprised of both the monomorphic SNPs and insertions/deletions identified by snippy, was generated incorporating our isolates (red font), as well as select isolates from the Ward et al (2016) (blue font) and Pang et al (2020) (green font) studies, and ST59 sequences downloaded from NCBI (black font). Molecular typing data was determined for the downloaded sequences, with IEC type identified for all isolates, and MES type for a random selection of isolates.…”

“… Maximum clade credibility tree showing the phylogenetic relationship between our ST59 isolates, along with global isolates from studies by Ward et al (2016) and Pang et al (2020) . Branch colors represent the 6 sub-lineages, with WGS-1 represented by gray, WGS-2 by purple, WGS-3 by orange, WGS-4 by pink, WGS-5 by blue and WGS-6 by green.…”

“…ST59 sequencing reads, for strains described by Ward et al (2016) , were downloaded from the European Nucleotide Archive repository and de novo assembly done as described. Contigs for strains described by Pang et al (2020) were downloaded from the National Center for Biotechnology Information (NCBI). HZW450 (CP020741), M013 (CP003166), SA957 (CP003603), SA268 (CP006630), and SA40 (CP003604) sequences were obtained from the National Center for Biotechnology Information (NCBI).…”

“…All six partitions used a 4-category gamma site model. All four SNP partitions shared a relaxed log normal clock model and each used an estimated Generalize Time Reversible substitution model similar to the analysis by Pang et al (2020) , while the insertions/deletions shared another relaxed log normal clock model and Mutation Death Model for substitution. The insertions and deletions in three PacBio assembled genomes (GD1409, GD1958, GD75) were masked due to observed likely high false positive rate.…”

“…Studies on the evolution of ST59 within Asia have noted that the lineage can be divided into 2 major clones, the Taiwan clone and the Asia-Pacific clone ( Huang et al, 2008 ), with observations that the Taiwan clone can cause severe infections and carries the PVL-encoding phage Sa2, while the Asia-Pacific clone is typically commensal and carries the Sa3 phage with staphylokinase ( Chen et al, 2013 ). Other studies have also examined the evolution and spread of ST59 within Taiwan and mainland China, describing sub clades within the regions differing in their carriage of mobile genetic elements related to multidrug resistance, immune evasion complex genes and SCC mec ( Hung et al, 2012 ; Pang et al, 2020 ). One of those mobile genetic elements is the Mobile Element Structure (MES), responsible for multidrug resistance and carrying genes conferring resistance to erythromycin, clindamycin, kanamycin, streptomycin, and chloramphenicol ( Hung et al, 2012 ).…”