Origin, evolution, and global transmission of community-acquired Staphylococcus aureus ST8

Area of Science:

• Microbiology
• Evolutionary Biology
• Genomics

Background:

• USA300 is a globally significant, hypervirulent community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) lineage.
• The evolutionary origins and dissemination pathways of USA300 have remained largely undetermined.
• Understanding USA300's evolution is critical for controlling its spread and impact.

Purpose of the Study:

• To reconstruct the molecular evolution and global dissemination history of Staphylococcus aureus multilocus sequence type (ST) 8, including the USA300 lineage.
• To identify the geographic origin and timeline of ST8 emergence and diversification.
• To elucidate the acquisition events of key USA300 genetic elements.

Main Methods:

• Comparative genomics of 224 diverse Staphylococcus aureus ST8 isolates.
• Analysis of core single nucleotide polymorphism (SNP) diversity.
• Assessment of accessory genome variations, including mobile genetic elements and phage integrations.

Main Results:

• The ancestor of ST8 Staphylococcus aureus likely originated in Central Europe in the mid-19th century.
• ST8 was exported to North America in the early 20th century, where it acquired USA300 defining elements: Panton-Valentine leukocidin (PVL), SCCmec IVa, and the ACME.
• USA300 subsequently spread globally from North America, with distinct clades identified in Africa, and earlier proposed ancestors were found to be distantly related.

Conclusions:

• The study clarifies the evolutionary trajectory of the pandemic USA300 lineage, tracing its origins to Central Europe and its subsequent global spread.
• Key virulence factors were acquired sequentially, primarily in North America, shaping the hypervirulent USA300 phenotype.
• The findings provide crucial insights into the population dynamics and historical dissemination of a major human pathogen.