Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis

ABSTRACT Staphylococcus aureus causes persistent clinical and subclinical bovine intramammary infections (IMI) worldwide. However, there is a lack of comprehensive information regarding genetic diversity, the presence of antimicrobial resistance (AMR), and virulence genes for S. aureus in bovine mil...

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Autores principales: Sohail Naushad, Diego B. Nobrega, S. Ali Naqvi, Herman W. Barkema, Jeroen De Buck
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:992a5bbd89994e72adb473d6c5560a892021-12-02T19:46:20ZGenomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis10.1128/mSystems.00063-202379-5077https://doaj.org/article/992a5bbd89994e72adb473d6c5560a892020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00063-20https://doaj.org/toc/2379-5077ABSTRACT Staphylococcus aureus causes persistent clinical and subclinical bovine intramammary infections (IMI) worldwide. However, there is a lack of comprehensive information regarding genetic diversity, the presence of antimicrobial resistance (AMR), and virulence genes for S. aureus in bovine milk in Canada. Here, we performed whole-genome sequencing (WGS) of 119 Canadian bovine milk S. aureus isolates and determined they belonged to 8 sequence types (ST151, ST352, ST351, ST2187, ST2270, ST126, ST133, and ST8), 5 clonal complexes (CC151, CC97, CC126, CC133, and CC8), and 18 distinct Spa types. Pan-, core, and accessory genomes were composed of 6,340, 1,279, and 2,431 genes, respectively. Based on phenotypic screening for AMR, resistance was common against beta-lactams (19% of isolates) and sulfonamides (7% of isolates), whereas resistance against pirlimycin, tetracycline, ceftiofur, and erythromycin and to the combination of penicillin and novobiocin was uncommon (3, 3, 3, 2, and 2% of all isolates, respectively). We also determined distributions of 191 virulence factors (VFs) in 119 S. aureus isolates after classifying them into 5 functional categories (adherence [n = 28], exoenzymes [n = 21], immune evasion [n = 20], iron metabolism [n = 29], and toxins [n = 93]). Additionally, we calculated the pathogenic potential of distinct CCs and STs and determined that CC151 (ST151 and ST351) had the highest pathogenic potential (calculated by subtracting core-VFs from total VFs), followed by CC97 (ST352 and ST2187) and CC126 (ST126 and ST2270), potentially linked to their higher prevalence in bovine IMI worldwide. However, there was no statistically significant link between the presence of VF genes and mastitis. IMPORTANCE Staphylococcus aureus is a major cause of bovine intramammary infections, leading to significant economic losses to dairy industry in Canada and worldwide. There is a lack of knowledge regarding genetic diversity, the presence of antimicrobial resistance (AMR), and virulence genes for S. aureus isolated from bovine milk in Canada. Based on whole-genome sequencing and genomic analysis, we have determined the phylogeny and diversity of S. aureus in bovine milk and concluded that it had a large accessory genome, limited distribution of AMR genes, variable VF gene profiles and sequence types (ST), and clonal complex (CC)-specific pathogenic potentials. Comprehensive information on the population structure, as well as the virulence and resistance characteristics of S. aureus from bovine milk, will allow for source attribution, risk assessment, and improved therapeutic approaches in cattle.Sohail NaushadDiego B. NobregaS. Ali NaqviHerman W. BarkemaJeroen De BuckAmerican Society for Microbiologyarticleintramammary infectionStaphylococcus aureuswhole-genome sequencingvirulence factorsantimicrobial resistance genessequence typesMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution DOAJ
collection DOAJ
language EN
topic intramammary infection
Staphylococcus aureus
whole-genome sequencing
virulence factors
antimicrobial resistance genes
sequence types
Microbiology
QR1-502
spellingShingle intramammary infection
Staphylococcus aureus
whole-genome sequencing
virulence factors
antimicrobial resistance genes
sequence types
Microbiology
QR1-502
Sohail Naushad
Diego B. Nobrega
S. Ali Naqvi
Herman W. Barkema
Jeroen De Buck
Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis
description ABSTRACT Staphylococcus aureus causes persistent clinical and subclinical bovine intramammary infections (IMI) worldwide. However, there is a lack of comprehensive information regarding genetic diversity, the presence of antimicrobial resistance (AMR), and virulence genes for S. aureus in bovine milk in Canada. Here, we performed whole-genome sequencing (WGS) of 119 Canadian bovine milk S. aureus isolates and determined they belonged to 8 sequence types (ST151, ST352, ST351, ST2187, ST2270, ST126, ST133, and ST8), 5 clonal complexes (CC151, CC97, CC126, CC133, and CC8), and 18 distinct Spa types. Pan-, core, and accessory genomes were composed of 6,340, 1,279, and 2,431 genes, respectively. Based on phenotypic screening for AMR, resistance was common against beta-lactams (19% of isolates) and sulfonamides (7% of isolates), whereas resistance against pirlimycin, tetracycline, ceftiofur, and erythromycin and to the combination of penicillin and novobiocin was uncommon (3, 3, 3, 2, and 2% of all isolates, respectively). We also determined distributions of 191 virulence factors (VFs) in 119 S. aureus isolates after classifying them into 5 functional categories (adherence [n = 28], exoenzymes [n = 21], immune evasion [n = 20], iron metabolism [n = 29], and toxins [n = 93]). Additionally, we calculated the pathogenic potential of distinct CCs and STs and determined that CC151 (ST151 and ST351) had the highest pathogenic potential (calculated by subtracting core-VFs from total VFs), followed by CC97 (ST352 and ST2187) and CC126 (ST126 and ST2270), potentially linked to their higher prevalence in bovine IMI worldwide. However, there was no statistically significant link between the presence of VF genes and mastitis. IMPORTANCE Staphylococcus aureus is a major cause of bovine intramammary infections, leading to significant economic losses to dairy industry in Canada and worldwide. There is a lack of knowledge regarding genetic diversity, the presence of antimicrobial resistance (AMR), and virulence genes for S. aureus isolated from bovine milk in Canada. Based on whole-genome sequencing and genomic analysis, we have determined the phylogeny and diversity of S. aureus in bovine milk and concluded that it had a large accessory genome, limited distribution of AMR genes, variable VF gene profiles and sequence types (ST), and clonal complex (CC)-specific pathogenic potentials. Comprehensive information on the population structure, as well as the virulence and resistance characteristics of S. aureus from bovine milk, will allow for source attribution, risk assessment, and improved therapeutic approaches in cattle.
format article
author Sohail Naushad
Diego B. Nobrega
S. Ali Naqvi
Herman W. Barkema
Jeroen De Buck
author_facet Sohail Naushad
Diego B. Nobrega
S. Ali Naqvi
Herman W. Barkema
Jeroen De Buck
author_sort Sohail Naushad
title Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis
title_short Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis
title_full Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis
title_fullStr Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis
title_full_unstemmed Genomic Analysis of Bovine <named-content content-type="genus-species">Staphylococcus aureus</named-content> Isolates from Milk To Elucidate Diversity and Determine the Distributions of Antimicrobial and Virulence Genes and Their Association with Mastitis
title_sort genomic analysis of bovine <named-content content-type="genus-species">staphylococcus aureus</named-content> isolates from milk to elucidate diversity and determine the distributions of antimicrobial and virulence genes and their association with mastitis
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/992a5bbd89994e72adb473d6c5560a89
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