Cargando…
Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis
BACKGROUND: Streptococcus uberis is one of the main causative agents of ovine mastitis, however little is known about this global, environmental pathogen and its genomic mechanisms of disease. In this study, we performed genomic analysis on 46 S. uberis isolates collected from mastitis-infected shee...
Autores principales: | , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9261030/ https://www.ncbi.nlm.nih.gov/pubmed/35799261 http://dx.doi.org/10.1186/s12917-022-03341-1 |
_version_ | 1784742178077016064 |
---|---|
author | Vezina, Ben Rosa, Maria Nives Canu, Antonella Tola, Sebastiana |
author_facet | Vezina, Ben Rosa, Maria Nives Canu, Antonella Tola, Sebastiana |
author_sort | Vezina, Ben |
collection | PubMed |
description | BACKGROUND: Streptococcus uberis is one of the main causative agents of ovine mastitis, however little is known about this global, environmental pathogen and its genomic mechanisms of disease. In this study, we performed genomic analysis on 46 S. uberis isolates collected from mastitis-infected sheep in Sardinia (Italy). RESULTS: Genomes were assigned into lineage clusters using PopPUNK, which found 27 distinct isolate clusters, indicating considerable genetic variability consistent with environmental isolates. Geographic trends were identified including regional linkage of several isolate clusters. Multi-locus Sequence Typing (MLST) performed poorly and provided no new insights. Genomes were then screened for antimicrobial resistance genes, which were compared to phenotypic resistance profiles. Isolates showed consistent phenotypic resistance to aminoglycosides with variable resistance to novobiocin and tetracycline. In general, identification of antimicrobial resistance genes did not correlate with phenotypic resistance profiles, indicating unknown genetic determinants. A multi-antimicrobial resistance cassette (aminoglycoside, lincosamide and streptogramin) was identified in the chromosome of three genomes, flanked by vestigial phage recombinases. This locus appears to have spread horizontally within discrete S. uberis populations within a 40 km radius (Sassari region). Genomes were screened for putative virulence factors, which identified 16 genes conserved between sheep and cow isolates, with no host-specific genes shared uniformly across all host-specific isolates. Pangenomic analysis was then performed to identify core genes which were putatively surface-exposed, for identification of potential vaccine targets. As all genomes encoded sortase, core genes were screened for the sortase cleavage motif. Of the 1445 core S. uberis genes, 64 were putative sortase substrates and were predominantly adhesins, permeases and peptidases, consistent with compounds found within ruminant milk such as xanthine, fibronectin and lactoferrin. CONCLUSIONS: This study demonstrated the importance of whole genome sequencing for surveillance of S. uberis and tracking horizontal acquisition of antimicrobial resistance genes, as well as providing insight into genetic determinants of disease, which cannot be inferred from the MLST schemes. Future mastitis surveillance should be informed by genomic analysis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12917-022-03341-1. |
format | Online Article Text |
id | pubmed-9261030 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-92610302022-07-07 Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis Vezina, Ben Rosa, Maria Nives Canu, Antonella Tola, Sebastiana BMC Vet Res Research BACKGROUND: Streptococcus uberis is one of the main causative agents of ovine mastitis, however little is known about this global, environmental pathogen and its genomic mechanisms of disease. In this study, we performed genomic analysis on 46 S. uberis isolates collected from mastitis-infected sheep in Sardinia (Italy). RESULTS: Genomes were assigned into lineage clusters using PopPUNK, which found 27 distinct isolate clusters, indicating considerable genetic variability consistent with environmental isolates. Geographic trends were identified including regional linkage of several isolate clusters. Multi-locus Sequence Typing (MLST) performed poorly and provided no new insights. Genomes were then screened for antimicrobial resistance genes, which were compared to phenotypic resistance profiles. Isolates showed consistent phenotypic resistance to aminoglycosides with variable resistance to novobiocin and tetracycline. In general, identification of antimicrobial resistance genes did not correlate with phenotypic resistance profiles, indicating unknown genetic determinants. A multi-antimicrobial resistance cassette (aminoglycoside, lincosamide and streptogramin) was identified in the chromosome of three genomes, flanked by vestigial phage recombinases. This locus appears to have spread horizontally within discrete S. uberis populations within a 40 km radius (Sassari region). Genomes were screened for putative virulence factors, which identified 16 genes conserved between sheep and cow isolates, with no host-specific genes shared uniformly across all host-specific isolates. Pangenomic analysis was then performed to identify core genes which were putatively surface-exposed, for identification of potential vaccine targets. As all genomes encoded sortase, core genes were screened for the sortase cleavage motif. Of the 1445 core S. uberis genes, 64 were putative sortase substrates and were predominantly adhesins, permeases and peptidases, consistent with compounds found within ruminant milk such as xanthine, fibronectin and lactoferrin. CONCLUSIONS: This study demonstrated the importance of whole genome sequencing for surveillance of S. uberis and tracking horizontal acquisition of antimicrobial resistance genes, as well as providing insight into genetic determinants of disease, which cannot be inferred from the MLST schemes. Future mastitis surveillance should be informed by genomic analysis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12917-022-03341-1. BioMed Central 2022-07-07 /pmc/articles/PMC9261030/ /pubmed/35799261 http://dx.doi.org/10.1186/s12917-022-03341-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Vezina, Ben Rosa, Maria Nives Canu, Antonella Tola, Sebastiana Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis |
title | Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis |
title_full | Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis |
title_fullStr | Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis |
title_full_unstemmed | Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis |
title_short | Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis |
title_sort | genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated streptococcus uberis |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9261030/ https://www.ncbi.nlm.nih.gov/pubmed/35799261 http://dx.doi.org/10.1186/s12917-022-03341-1 |
work_keys_str_mv | AT vezinaben genomicsurveillancerevealsantibioticresistancegenetransmissionviaphagerecombinaseswithinsheepmastitisassociatedstreptococcusuberis AT rosamarianives genomicsurveillancerevealsantibioticresistancegenetransmissionviaphagerecombinaseswithinsheepmastitisassociatedstreptococcusuberis AT canuantonella genomicsurveillancerevealsantibioticresistancegenetransmissionviaphagerecombinaseswithinsheepmastitisassociatedstreptococcusuberis AT tolasebastiana genomicsurveillancerevealsantibioticresistancegenetransmissionviaphagerecombinaseswithinsheepmastitisassociatedstreptococcusuberis |