Abstract:
Most new pathogens of humans and animals arise via switching events from distinct
host species. However, our understanding of the evolutionary and ecological drivers of
successful host adaptation, expansion, and dissemination are limited. Staphylococcus
aureus is a major bacterial pathogen of humans and a leading cause of mastitis in dairy
cows worldwide. Here we trace the evolutionary history of bovine S. aureus using a global
dataset of 10,254 S. aureus genomes including 1,896 bovine isolates from 32 countries
in 6 continents. We identified 7 major contemporary endemic clones of S. aureus causing
bovine mastitis around the world and traced them back to 4 independent host-jump
events from humans that occurred up to 2,500 y ago. Individual clones emerged and
underwent clonal expansion from the mid-19th to late 20th century coinciding with
the commercialization and industrialization of dairy farming, and older lineages have
become globally distributed via established cattle trade links. Importantly, we identified
lineage-dependent differences in the frequency of host transmission events between
humans and cows in both directions revealing high risk clones threatening veterinary and
human health. Finally, pangenome network analysis revealed that some bovine S. aureus
lineages contained distinct sets of bovine-associated genes, consistent with multiple
trajectories to host adaptation via gene acquisition. Taken together, we have dissected
the evolutionary history of a major endemic pathogen of livestock providing a comprehensive
temporal, geographic, and gene-level perspective of its remarkable success.
