Journal Article

Time-calibrated phylogenetic and chromosomal mobilome analyses of Staphylococcus aureus CC398 reveal geographical and host-related evolution

Overesch, Gudrun, Perreten, Vincent, Egli, Adrian, Fernandez, Javier Eduardo

2024

Overview

An international collection of Staphylococcus aureus of clonal complex (CC) 398 from diverse hosts spanning all continents and a 30 year-period is studied based on whole-genome sequencing (WGS) data. The collection consists of publicly available genomic data from 2994 strains and 134 recently sequenced Swiss methicillin-resistant S. aureus (MRSA) CC398 strains. A time-calibrated phylogeny reveals the presence of distinct phylogroups present in Asia, North and South America and Europe. European MRSA diverged from methicillin-susceptible S. aureus (MSSA) at the beginning of the 1950s. Two major European phylogroups (EP4 and EP5), which diverged approximately 1974, are the main drivers of MRSA CC398 spread in Europe. Within EP5, an emergent MRSA lineage spreading among the European horse population (EP5-Leq) diverged approximately 1996 from the pig lineage (EP5-Lpg), and also contains human-related strains. EP5-Leq is characterized by staphylococcal cassette chromosome mec (SCC mec ) IVa and spa type t011 (CC398-IVa-t011), and EP5-Lpg by CC398-SCC mec Vc-t011. The lineage-specific antibiotic resistance and virulence gene patterns are mostly mediated by the acquisition of mobile genetic elements like SCC mec , S. aureus Genomic Islands (SaGIs), prophages and transposons. Different combinations of virulence factors are present on S. aureus pathogenicity islands (SaPIs), and novel antimicrobial resistance gene containing elements are associated with certain lineages expanding in Europe. This WGS-based analysis reveals the actual evolutionary trajectory and epidemiological trend of the international MRSA CC398 population considering host, temporal, geographical and molecular factors. It provides a baseline for global WGS-based One-Health studies of adaptive evolution of MRSA CC398 as well as for local outbreak investigations. Authors perform a whole genome sequencing-based analysis of an international MRSA CC398 population, revealing the evolutionary trajectory and epidemiological trend considering host, temporal, geographical and molecular factors as well as lineage-associated mobile genetic elements.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 45 / 45/23 / 631/326/1320 / 631/326/325/2482 / 631/326/41/2529 / Animal populations / Animals / Antibiotic resistance / Antimicrobial resistance / Chromosomes / Chromosomes, Bacterial - genetics / Drug resistance / Epidemiology / Europe - epidemiology / Evolution / Evolution & development / Evolution, Molecular / Gene sequencing / Genome, Bacterial / Genomes / Genomic analysis / Genomic islands / Horses - microbiology / Humanities and Social Sciences / Humans / Islands / Methicillin / Methicillin-Resistant Staphylococcus aureus - classification / Methicillin-Resistant Staphylococcus aureus - genetics / Methicillin-Resistant Staphylococcus aureus - isolation & purification / Methicillin-Resistant Staphylococcus aureus - pathogenicity / multidisciplinary / Pathogenicity / Pathogenicity islands / Pathogens / Phylogeny / Prophages / Science / Science (multidisciplinary) / Staphylococcal Infections - epidemiology / Staphylococcal Infections - microbiology / Staphylococcus aureus / Staphylococcus aureus - classification / Staphylococcus aureus - genetics / Staphylococcus aureus - pathogenicity / Staphylococcus infections / Swine / Transposons / Virulence / Virulence factors / Virulence Factors - genetics / Whole Genome Sequencing