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Distinct phenotypic traits of Staphylococcus aureus are associated with persistent, contagious bovine intramammary infections.

ABSTRACT: Staphylococcus aureus causing persistent, recurrent bovine intramammary infections are still a major challenge to dairy farming. Generally, one or a few clonal lineages are predominant in dairy herds, indicating animal-to-animal transfers and the existence of distinct pathotypic traits. The aim of this study was to determine if long term persistence and spreading of S. aureus are associated with specific phenotypic traits, including cellular invasion, cytotoxicity and biofilm formation. Mastitis isolates were collected over a 3-years period from a single dairy herd, resulting in two persistent subtypes, the high within-herd prevalent subtype ST9 (CC9)-methicillin-susceptible S. aureus (MSSA), designated HP/ST9, and the low within-herd prevalent subtype ST504 (CC705)-MSSA, designated LP/ST504. Characterization of the two different coexisting persistent subtypes showed that the following phenotypic traits are particularly associated with high within-herd prevalence: lack of capsular polysaccharide expression, high cellular invasiveness, low cytotoxicity and high biofilm/ poly-N-acetylglucosamine (PNAG) production, which may concomitantly contribute to the spreading of HP/ST9 within the herd. By contrast to HP/ST9, LP/ST504 is characterized by the formation of colony dendrites, which may help the bacteria to access deeper tissues as niches for persistence in single animals. Thus, within a single herd, two different types of persistence can be found in parallel, allowing longtime persistence of S. aureus in dairy cattle. Furthermore, this study indicates that ST9 (CC9)-MSSA strains, which are currently thought to have their primary reservoir in swine and humans, can also successfully spread to new hosts and persist in dairy herds for years.

SUBMITTER: Grunert T

PROVIDER: S-EPMC6206001 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Distinct phenotypic traits of Staphylococcus aureus are associated with persistent, contagious bovine intramammary infections.

Grunert Tom T Stessl Beatrix B Wolf Franz F Sordelli Daniel O DO Buzzola Fernanda R FR Ehling-Schulz Monika M

Scientific reports 20181029 1

Staphylococcus aureus causing persistent, recurrent bovine intramammary infections are still a major challenge to dairy farming. Generally, one or a few clonal lineages are predominant in dairy herds, indicating animal-to-animal transfers and the existence of distinct pathotypic traits. The aim of this study was to determine if long term persistence and spreading of S. aureus are associated with specific phenotypic traits, including cellular invasion, cytotoxicity and biofilm formation. Mastitis ...[more]

PMID: 30374136

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Project description:BACKGROUND: Streptococcus spp. and other Gram-positive, catalase-negative cocci (PNC) form a large group of microorganisms which can be found in the milk of cows with intramammary infection. The most frequently observed PNC mastitis pathogens (major pathogens) are Streptococcus uberis, Strep. dysgalactiae, and Strep. agalactiae. The remaining PNC include a few minor pathogens and a large nonpathogenic group. Improved methods are needed for the accurate identification and differentiation of PNC. A total of 151 PNC were collected from cows with intramammary infection and conclusively identified by 16S rRNA sequencing as reference method. Nine phenotypic microbiological tests (alpha-hemolysis, CAMP reaction, esculin hydrolysis, growth on kanamycin esculin azide agar and on sodium chloride agar, inulin fermentation, hippurate hydrolysis, leucine aminopeptidase and pyrrolidonyl peptidase activity), multiplex PCR for the three major pathogens (target genes for Strep. uberis, Strep. dysgalactiae and Strep. agalactiae: pauA, 16S rRNA, and sklA3, respectively), and mass spectroscopy using the matrix-assisted laser desorption ionization-time of flight (MALDI-TOF MS) were evaluated for the diagnosis and discrimination of the three clinically most relevant PNC. RESULTS: The probability that a strain of Strep. uberis, Strep. dysgalactiae and Strep. agalactiae was correctly identified by combining the results of the 9 phenotypic tests was 92%, 90%, and 100%, respectively. Applying the multiplex PCR, all strains of the three major pathogens were correctly identified and no false positive results occurred. Correct identification was observed for all strains of Strep. uberis and Strep. agalactiae using MALDI-TOF MS. In the case of Strep. dysgalactiae, some variability was observed at the subspecies level, but all strains were allocated to one single cluster. CONCLUSIONS: The results of the present study show that reliable identification of the clinically most relevant PNC (Strep. uberis, Strep. agalactiae and Strep. dysgalactiae) can be obtained by use of a combination of colony morphology, hemolysis type and catalase reaction, and a multiplex PCR with specific primers restricted to these 3 pathogens. The MALDI-TOF MS is a fast method that shows promising results, although identification of Strep. dysgalactiae at the subspecies level is not yet satisfactory.

Project description:BACKGROUND:Coagulase-negative staphylococci (CoNS) are among the leading bacterial causes of bovine mastitis in many dairy-producing countries. Among the challenges associated with the specific diagnosis of CoNS infections is the biochemical heterogeneity of the species in the genus and the unavailability of accurate, cost-effective and up-to-date diagnostic tests. A previous study investigating the diversity of CoNS associated with cases of bovine mastitis in South Africa, resulted in six CoNS isolates which could not be identified despite the use of a combination of different molecular assays. The identification and characterisation of the isolates was pursued further in this study. RESULTS:The six CoNS isolates in question were identified by sequencing multiple housekeeping genes (dnaJ, hsp60, rpoB, 16S rRNA) and characterized through the use of matrix-assisted laser/desorption ionization time of flight mass spectrometry (MALDI-TOF MS) and the Biolog GEN III Microplate™ bacterial identification system. Sequencing of housekeeping genes identified the isolates as S. devriesei. This Staphylococcus species was only described in 2010 and this is the first report documenting the isolation of S. devriesei from cases of bovine IMIs in South Africa. Analysis of mass spectra generated by the six isolates showed intra-species variation which was also observed when evaluating the metabolic profiles of the isolates using the Biolog GEN III system. Neither the MALDI-TOF MS nor the Biolog database are currently populated with data relating to S. devriesei, resulting in the isolates not being identified, in the case of MALDI-TOF MS analysis, or mis-identified as was observed with the Biolog GEN III system. CONCLUSIONS:The phenotyping data collected during this investigation provides useful information concerning Staphylococcus devriesei which could be used to populate user system databases thereby ensuring the accurate identification of isolates in future. The availability of improved diagnostics will in turn facilitate studies to elucidate the epidemiology, pathogenicity and true prevalence of this species in dairy herds.

Project description:Staphylococcus aureus is one of the major pathogens responsible for intramammary infections in small ruminants, causing severe economic losses in dairy farms. In addition, S. aureus can contaminate milk and dairy products and produce staphylococcal enterotoxins, being responsible for staphylococcal food poisoning. Currently, data on the population structure and the virulence gene patterns of S. aureus strains isolated from goat milk is limited. Therefore, this study aimed at defining Ribosomal Spacer PCR (RS-PCR) genotypes, clonal complexes (CC), spa types, and virulence gene profiles of S. aureus isolated from goat milk samples from Lombardy region of Italy. A total of 295 S. aureus isolates from 65 goat bulk tank milk samples were genotyped by RS-PCR. spa typing and virulence gene patterns of a subgroup of 88 isolates were determined, and MLST was performed on a further subgroup of 39 isolates, representing all the spa types identified during the analysis. This study revealed 7 major genotypic clusters (CLR, CLAA, CLZ, CLAW, CLBW, CLS, and CLI), of which S. aureus CLR (19.8%) was the most common. A total of 26 different spa types were detected, the most prevalent types were t1773 (24%), t5428 (22.7%), and t2678 (12.5%). Overall, 44.3% of all isolates harbored at least one enterotoxin gene. The most prevalent was the combination of sec-sel genes (35.2%). Based on their MLST, isolates were assigned to 14 different CC, with majority grouped as CC133 (24%), CC130 (19.6%), and CC522 (19.6%). The caprine S. aureus population was depicted with a minimum spanning tree and an evolutionary analysis based on spa typing and MLST, respectively. Then, the variability of such strains was compared to that of bovine strains isolated in the same space-time span. Our results confirmed that S. aureus isolates from goats have wide genetic variability and differ from the bovine strains, supporting the idea that S. aureus from small ruminants may constitute a distinct population.

Dataset Information

Distinct phenotypic traits of Staphylococcus aureus are associated with persistent, contagious bovine intramammary infections.

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Distinct phenotypic traits of Staphylococcus aureus are associated with persistent, contagious bovine intramammary infections.

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