Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray

Abstract

Staphylococcus aureus is a commensal and pathogen of several mammalian species, particularly humans and cattle. We aimed to (i) identify S. aureus genes associated with host specificity, (ii) determine the relatedness of human and animal isolates, and (iii) identify whether human and animal isolates typically exchanged mobile genetic elements encoding virulence and resistance genes. Using a well-validated seven-strain S. aureus microarray, we compared 56 UK S. aureus isolates that caused infection in cows, horses, goats, sheep and a camel with 161 human S. aureus isolates from healthy carriers and community acquired infections in the UK. We had previously shown that human isolates are clustered into ten dominant and a few minor lineages, each with unique combinations of surface proteins predicted to bind to human proteins. We found that the animal-associated S. aureus clustered into ten lineages, with 61 % assigned to four lineages, ST151, ST771, ST130 and ST873, that were unique to animals. The majority of bovine mastitis was caused by isolates of lineage ST151, ST771 and ST97, but a few human lineages also caused mastitis. S. aureus isolated from horses were more likely to cluster into humanassociated lineages, with 54 % of horse-associated S. aureus assigned to the human clusters CC1, CC8 and CC22; along with the presence of some multi-drug resistant strains, this suggests a human origin. This is the most comprehensive genetic comparison of human versus animal S. aureus isolates conducted, and because we used a whole-genome approach we could estimate the key genes with the greatest variability that are associated with host specificity. Several genes conserved in all human isolates were variable or missing in one or more animal lineages, including the well-characterized lineage specific genes fnbA, fnbB and coa. Interestingly, genes carried on mobile genetic elements (MGEs) such as chp, scn and sak were less common in animal S. aureus isolates, and bap was not found. There was a lot of MGE variation within lineages, and some evidence that exchange of MGEs such as bacteriophage and pathogenicity islands between animal and human lineages is feasible, but there was less evidence of antibiotic resistance gene transfer on the staphylococcal cassette chromosomes (SCC) or plasmids. Surprisingly, animal lineages are closely related to human lineages and only a handful of genes or gene combinations may be responsible for host specificity.

Characterization of Dutch Staphylococcus aureus from bovine mastitis using a Multiple Locus Variable Number Tandem Repeat Analysis

“…SIRU05 was analyzed more in depth, since it could not be amplified in any of the bovine isolates including 4 isolates with ST97 that were already known as possibly human derived (Smith et al, 2005a;Sung et al, 2008). PCR of the region neighboring SIRU05 demonstrated that all isolates were fragment A and B positive.…”

Host adaptation of bovine Staphylococcus aureus seems associated with bacteriological cure after lactational antimicrobial treatment

“…Some sequence types (ST) such as ST398 are found in many host species, including humans and animals (Weese and van Duijkeren, 2010), whereas other types of Staph. aureus are specifically associated with animals (Sung et al, 2008;Ikawaty et al, 2009;Lowder et al, 2009). Bovineassociated Staph.…”

Phenogenotyping of Closely Related Methicillin Resistant Staphylococcus aureus Isolated from Milk and Meat Products

“…It was estimated that over 60% of the emerging human pathogens come from animals [1] and food products [2]. The minority of S. aureus strains obtained from food products are not host specific and consumption of these contaminated feed leads to colonization of S. aureus in humans causing community acquired infections [3][4][5]. In addition, developed resistance to methicillin limits the use of β-lactam antimicrobials and the antibiogram schemes were often uninformative for typing many strains [6].…”