Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock

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.

Genomic Characterization of Staphylococcus aureus in Wildlife

“…However, all the strains belonging to these sequence types in the present study were MSSA. The ability of CC130 to transition across several host species has been demonstrated by the numerous spillover events from humans and sheep that lead to the contemporary bovine isolates of CC130 [ 48 ]. In fact, Loncaric et al [ 49 ] found the same strain in a wild hare, a cow, and a sheep sharing the same habitat, which suggests an exchange may occur.…”

Molecular Epidemiology and Characterization of Multidrug-Resistant MRSA ST398 and ST239 in Himachal Pradesh, India

“… 26 Genetically diverse MRSA is primarily characterized by the serial emergency of epidemic human host clones which are CC130, CC425, CC121, CC8 and CC97. 27 Although prevalence has declined, attention is particularly necessary as this remains a formidable clinical threat. 28 Regular surveillance with accurate detection of such MRSA strains is therefore important so that appropriate antimicrobial therapy may be given to the patients, understand the evolution for the control of the nosocomial spread and preventive measures of these strains.…”

Comparison of genomic diversity between single and pooled Staphylococcus aureus colonies isolated from human colonization cultures

“…and osteomyelitis [23,24]. As with other prominent pathogens, WGS has significantly improved S. aureus epidemiological studies, and our ability to track the spread of antibiotic resistance and virulence across populations [3,[25][26][27][28][29]. Here, we used samples from human participants who had an index methicillin-resistant S. aureus (MRSA) skin and soft tissue infection (SSTI) as part of an ongoing study, SEMAPHORE (Study of the Evolution of MRSA, Antibiotics and Persistence Having the Outcome of Recurrence).…”

“…As with other prominent pathogens, WGS has significantly improved S. aureus epidemiological studies, and our ability to track the spread of antibiotic resistance and virulence across populations [3, 25–29]. Here, we used samples from human participants who had an index methicillin-resistant S.…”