Molecular Characterization of Staphylococcus aureus Isolated from Bovine Mastitis and Close Human Contacts in South African Dairy Herds: Genetic Diversity and Inter-Species Host Transmission.

Tracy Schmidt,Marleen M Kock,Marthie M Ehlers

doi:10.3389/fmicb.2017.00511

Abstract

Staphylococcus aureus is one of the most common etiological agents of contagious bovine mastitis worldwide. The purpose of this study was to genetically characterize a collection of S. aureus isolates (bovine = 146, human = 12) recovered from cases of bovine mastitis and nasal swabs of close human contacts in the dairy environment. Isolates were screened for a combination of clinically significant antimicrobial and virulence gene markers whilst the molecular epidemiology of these isolates and possible inter-species host transmission was investigated using a combination of genotyping techniques. None of the isolates under evaluation tested positive for methicillin or vancomycin resistance encoding genes. Twenty seven percent of the bovine S. aureus isolates tested positive for one or more of the pyrogenic toxin superantigen (PTSAg) genes with the sec and sell genes predominating. Comparatively, 83% of the human S. aureus isolates tested positive for one or more PTSAg genes with a greater variety of genes being detected. Genomic DNA macrorestriction followed by pulsed-field gel electrophoresis (PFGE) of the bovine isolates generated 58 electrophoretic patterns which grouped into 10 pulsotypes at an 80% similarity level. The majority of the bovine isolates, 93.2% (136/146), clustered into four major pulsotypes. Seven sequence types (ST) were identified among the representative bovine S. aureus isolates genotyped, including: ST8 (CC8), ST97 (CC97), ST351 (CC705), ST352 (CC97), ST508 (CC45), ST2992 (CC97) and a novel sequence type, ST3538 (CC97). Based on PFGE analysis, greater genetic diversity was observed among the human S. aureus isolates. Bovine and human isolates from three sampling sites clustered together and were genotypically indistinguishable. Two of the isolates, ST97 and ST352 belong to the common bovine lineage CC97, and their isolation from close human contacts suggests zoonotic transfer. In the context of this study, the third isolate, ST8 (CC8), is believed to be a human clone which has transferred to a dairy cow and has subsequently caused mastitis. The detection of indistinguishable S. aureus isolates from bovine and human hosts at three of the sampling sites is suggestive of bacterial transmission and supports the need for vigilant monitoring of staphylococcal populations at the human-animal interface.

Highlights

Staphylococcus aureus is a versatile pathogen responsible for a variety of infections in humans and animals (Hata et al, 2008)
The production of enterotoxins is significant from a public health standpoint as the ingestion of preformed toxins is a major cause of food poisoning worldwide (Le Loir et al, 2003; Srinivasan et al, 2006)
This study presents the first insight into the virulence characteristics and genetic diversity of S. aureus strains causing mastitis in dairy herds in a province of South Africa

Summary

Introduction

Staphylococcus aureus is a versatile pathogen responsible for a variety of infections in humans and animals (Hata et al, 2008). Through the production of toxins, S. aureus can cause specific toxin-mediated conditions, such as scalded skin syndrome, staphylococcal food poisoning and toxic shock syndrome (Becker et al, 2015). Most S. aureus strains are able to produce one or more pyrogenic toxin superantigens (PTSAgs) which includes staphylococcal enterotoxins and the structurally related protein, toxic shock syndrome toxin-1 (TSST1) (Wright and Novick, 2003). All of these toxins exhibit superantigenic activity by interacting with antigen-presenting cells and T-lymphocytes irrespective of the antigen specificity of the cells (Akineden et al, 2001; Argudín et al, 2010). The expression of most staphylococcal virulence factors occurs in a co-ordinated manner and is strictly controlled by a series of regulatory genes which operate under the control of the accessory gene regulator (agr) (Ben Ayed et al, 2008; Lowy, 2013)

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