Staphylococcus aureus bovine-adapted lineage CC97 is associated with farms with a high within-herd prevalence of subclinical mastitis in Ireland.

Bovine IMI has a negative impact on the dairy industry through economic loss, increased antibiotic use, and reduced animal welfare. Major infectious agents include Staphylococcus aureus, non-aureus staphylococci and mammaliicocci (NASM), streptococci, and coliforms such as Escherichia coli, with the pathogen profile influenced by geography and production system. Strain variability, particularly for S. aureus, also affects the severity and epidemiology of IMI. To investigate the genetic variability of bovine S. aureus and determine if herd-level and individual cow milk quality parameters are associated with specific IMI pathogens or S. aureus genotypes, 20 Irish dairy herds were studied. These herds were classified as problem herds, that is, high within-herd prevalence of subclinical mastitis based on cow-level SCC (n = 10), or control, that is, low within-herd prevalence of subclinical mastitis (n = 10). Milk samples were collected from putatively infected primiparous and multiparous cows and subjected to microbiological, milk composition, and milk processing analyses. The major pathogens isolated were NASM (37%), streptococci (17%), and S. aureus (13%), with no microorganism recovered from 29% of samples. The majority of S. aureus isolates belonged to clonal complex (CC) 97 or CC151, and S. aureus lineage was significantly associated with farm status; CC97 was 10 times more likely to be isolated from a problem than a control herd, whereas CC151 was 5.6 times more likely to be recovered from a control than a problem herd. The SCC was dependent on the nature of the infecting agent. For all bacterial species, positive samples had significantly higher SCC than samples that were bacteriologically negative, with milk containing S. aureus having significantly higher SCC than all other groups. Infectious agent was also associated with TS, lactose percentage, and rennet coagulation time, although there were no differences between S. aureus lineages in SCC, milk composition, or processing parameters. Antimicrobial resistance was rare among the S. aureus isolates, although CC97 and CC8 isolates were resistant to penicillin and ampicillin. Comparative genomic analysis of the S. aureus isolates identified lineage-associated virulence genes. Pan-genome analysis identified a small number of CC97 and CC151 unique genes, although no functional enrichment of the unique genes was identified. A number of the lineage-unique genes were associated with mobile genetic elements.