Staphylococcus aureus host range and human-bovine host shift

Abstract

Staphylococcus aureus is a major agent of bovine mastitis. The concomitant emergence of pig-associated methicillin-resistant S. aureus (MRSA) in human carriage and infection requires a reexamination of the host range and specificity of human- and cow-associated S. aureus strains, something which has not been systematically studied previously. The genetic relatedness of 500 S. aureus isolates from bovine mastitis cases, 57 isolates from nasal carriage of farmers, and 133 isolates from nonfarmers was determined by amplified fragment length polymorphism (AFLP) analysis and spa typing. Multilocus sequence typing (MLST) was conducted on a subset of isolates to match AFLP clusters with MLST clonal complexes (CCs). This data set allowed us to study host range and host specificity and to estimate the extent of bovine-to-human transmission. The genotype compositions of S. aureus isolates from farmers and nonfarmers were very similar, while the mastitis isolates were quite distinct. Overall, transmission was low, but specific genotypes did show increased cow-to-human transmission. Unexpectedly, more than one-third of mastitis isolates belonged to CC8, a lineage which has not been considered to be bovine mastitis associated, but it is well known from human carriage and infection (i.e., USA300). Despite the fact that we did detect some transmission of other genotypes from cows to farmers, no transmission of CC8 isolates to farmers was detected, except for one tentative case. This was despite the close genetic relatedness of mastitis CC8 strains to nonfarmer carriage strains. These results suggest that the emergence of the new bovine-adapted genotype was due to a recent host shift from humans to cows concurrent with a loss of the ability to colonize humans. More broadly, our results indicate that host specificity is a lineage-specific trait that can rapidly evolve.

Fig. 1.

Clustering of selected AFLP data by a 50% consensus Bayesian tree. For clarity, only selected isolates are included: isolates from nonfarmers (n = 47), all isolates from farmers (n = 60), all bovine mastitis isolates which were genotyped by MLST (n = 31), bovine isolates where human-to-animal transmission was suspected (n = 13), and a random sample of other bovine mastitis isolates (n = 30). Filled symbols indicate the isolates that were genotyped by MLST. The isolates for which human-to-bovine transmission was suspected are labeled with the farm number and M for bovine mastitis isolates or F for farmer isolates. The posterior probability (a proportion of trees supporting a given branch) is indicated in italics.

Fig. 2.

Genotype composition of S. aureus isolates from cases of bovine mastitis and from human carriers. One isolate per farm and sampling time is included. The colors represent clusters defined by AFLP analysis.

Fig. 3.

Approximate geographic position (based on postal codes) of the studied farms and the genotypes of S. aureus bovine mastitis isolates. Colors represent the genotypes of the isolates, as defined by AFLP analysis. The size of the circle indicates the number isolates from a given farm. The smallest circles indicate a single isolate. The data for the first available sampling time are shown for each farm. The circles representing farms where the farmers were sampled are indicated by thicker black lines. The farms where MRSA was found at any sampling time are indicated by thick purple lines.

Fig. 4.

Within-farm prevalence of isolates from different clusters. Averages and standard deviations are shown. The colors indicate clusters as defined by AFLP analysis.