1887

Abstract

is a globally endemic and poorly controlled cause of bovine mastitis impacting the sustainability of the modern dairy industry. A core genome was derived from 579 newly sequenced isolates, along with 305 publicly available genome sequences of isolated from 11 countries around the world and used to develop a core genome multi-locus sequence typing (cgMLST) scheme. The core genome comprised 1475 genes, and these were used to identify 1447 curated loci that were indexed into the cgMLST scheme. This was able to type 1012 of 1037 (>97  %) isolates used and differentiated the associated sequences into 932 discrete core genome sequence types (cgSTs). Analysis of the phylogenetic relationships of cgSTs revealed no clear clustering of isolates based on metadata such as disease status or year of isolation. Geographical clustering of cgSTs was limited to identification of a UK-centric clade, but cgSTs from UK isolates were also dispersed with those originating from other geographical regions across the entire phylogenetic topology. The cgMLST scheme offers a new tool for the detailed analysis of this globally important pathogen of dairy cattle. Initial analysis has re-emphasized and exemplified the genetically diverse nature of the global population of this opportunistic pathogen.

Funding
This study was supported by the:
  • Dechra Pharmaceuticals
    • Principle Award Recipient: JamesLeigh
  • Biotechnology and Biological Sciences Research Council (Award BB/T001933/1)
    • Principle Award Recipient: JamesLeigh
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001225
2024-03-21
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/3/mgen001225.html?itemId=/content/journal/mgen/10.1099/mgen.0.001225&mimeType=html&fmt=ahah

References

  1. Bradley AJ, Leach KA, Breen JE, Green LE, Green MJ. Survey of the incidence and aetiology of mastitis on dairy farms in England and Wales. Vet Rec 2007; 160:253–257 [View Article] [PubMed]
    [Google Scholar]
  2. Davies PL, Leigh JA, Bradley AJ, Archer SC, Emes RD et al. Molecular epidemiology of Streptococcus uberis clinical mastitis in dairy herds: strain heterogeneity and transmission. J Clin Microbiol 2016; 54:68–74 [View Article] [PubMed]
    [Google Scholar]
  3. Jayarao BM, Bassam BJ, Caetano-Anollés G, Gresshoff PM, Oliver SP. Subtyping of Streptococcus uberis by DNA amplification fingerprinting. J Clin Microbiol 1992; 30:1347–1350 [View Article] [PubMed]
    [Google Scholar]
  4. Wieliczko RJ, Williamson JH, Cursons RT, Lacy-Hulbert SJ, Woolford MW. Molecular typing of Streptococcus uberis strains isolated from cases of bovine mastitis. J Dairy Sci 2002; 85:2149–2154 [View Article] [PubMed]
    [Google Scholar]
  5. Phuektes P, Mansell PD, Dyson RS, Hooper ND, Dick JS et al. Molecular epidemiology of Streptococcus uberis isolates from dairy cows with mastitis. J Clin Microbiol 2001; 39:1460–1466 [View Article] [PubMed]
    [Google Scholar]
  6. Jayarao BM, Schilling EE, Oliver SP. Genomic deoxyribonucleic acid restriction fragment length polymorphism of Streptococcus uberis: evidence of clonal diversity. J Dairy Sci 1993; 76:468–474 [View Article] [PubMed]
    [Google Scholar]
  7. Gilbert FB, Fromageau A, Lamoureux J, Poutrel B. Evaluation of tandem repeats for MLVA typing of Streptococcus uberis isolated from bovine mastitis. BMC Vet Res 2006; 2:33 [View Article] [PubMed]
    [Google Scholar]
  8. Hill AW, Brady CA. A note on the isolation and propagation of lytic phages from Streptococcus uberis and their potential for strain typing. J Appl Bacteriol 1989; 67:425–431 [View Article] [PubMed]
    [Google Scholar]
  9. Lämmler C. Biochemical and serological properties of Streptococcus uberis. Zentralbl Veterinarmed B 1991; 38:737–742 [View Article] [PubMed]
    [Google Scholar]
  10. Liu S, Li X, Guo Z, Liu H, Sun Y et al. A core genome multilocus sequence typing scheme for Streptococcus mutans. mSphere 2020; 5:e00348-20 [View Article] [PubMed]
    [Google Scholar]
  11. Silva NCC, Yang Y, Rodrigues MX, Tomazi T, Bicalho RC. Whole-genome sequencing reveals high genetic diversity of Streptococcus uberis isolated from cows with mastitis. BMC Vet Res 2021; 17:321 [View Article] [PubMed]
    [Google Scholar]
  12. Coffey TJ, Pullinger GD, Urwin R, Jolley KA, Wilson SM et al. First insights into the evolution of Streptococcus uberis: a multilocus sequence typing scheme that enables investigation of its population biology. Appl Environ Microbiol 2006; 72:1420–1428 [View Article] [PubMed]
    [Google Scholar]
  13. Vezina B, Rosa MN, Canu A, Tola S. Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis. BMC Vet Res 2022; 18:264 [View Article] [PubMed]
    [Google Scholar]
  14. Rosa NM, Duprè I, Azara E, Longheu CM, Tola S. Molecular typing and antimicrobial susceptibility profiles of Streptococcus uberis isolated from sheep milk. Pathog 2021; 10:1489 [View Article] [PubMed]
    [Google Scholar]
  15. Vezina B, Al-Harbi H, Ramay HR, Soust M, Moore RJ et al. Sequence characterisation and novel insights into bovine mastitis-associated Streptococcus uberis in dairy herds. Sci Rep 2021; 11:3046 [View Article] [PubMed]
    [Google Scholar]
  16. Käppeli N, Morach M, Zurfluh K, Corti S, Nüesch-Inderbinen M et al. Sequence types and antimicrobial resistance profiles of Streptococcus uberis isolated from bovine mastitis. Front Vet Sci 2019; 6:234 [View Article] [PubMed]
    [Google Scholar]
  17. Reyes J, Rodriguez-Lecompte JC, Blanchard A, McClure JT, Sánchez J. Molecular variability of Streptococcus uberis isolates from intramammary infections in Canadian dairy farms from the Maritime region. Can J Vet Res 2019; 83:168–176 [PubMed]
    [Google Scholar]
  18. Tomita T, Meehan B, Wongkattiya N, Malmo J, Pullinger G et al. Identification of Streptococcus uberis multilocus sequence types highly associated with mastitis. Appl Environ Microbiol 2008; 74:114–124 [View Article] [PubMed]
    [Google Scholar]
  19. McInerney JO, McNally A, O’Connell MJ. Why prokaryotes have pangenomes. Nat Microbiol 2017; 2:17040 [View Article] [PubMed]
    [Google Scholar]
  20. Maiden MCJ, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 2013; 11:728–736 [View Article] [PubMed]
    [Google Scholar]
  21. Abdel-Glil MY, Chiaverini A, Garofolo G, Fasanella A, Parisi A et al. A whole-genome-based gene-by-gene typing system for standardized high-resolution strain typing of Bacillus anthracis. J Clin Microbiol 2021; 59:e0288920 [View Article] [PubMed]
    [Google Scholar]
  22. Cody AJ, Bray JE, Jolley KA, McCarthy ND, Maiden MCJ. Core genome multilocus sequence typing scheme for stable, comparative analyses of Campylobacter jejuni and C. coli human disease isolates. J Clin Microbiol 2017; 55:2086–2097 [View Article] [PubMed]
    [Google Scholar]
  23. Gonzalez-Escalona N, Jolley KA, Reed E, Martinez-Urtaza J. Defining a core genome multilocus sequence typing scheme for the global epidemiology of Vibrio parahaemolyticus. J Clin Microbiol 2017; 55:1682–1697 [View Article] [PubMed]
    [Google Scholar]
  24. Liang KYH, Orata FD, Islam MT, Nasreen T, Alam M et al. A Vibrio cholerae core genome multilocus sequence typing scheme to facilitate the epidemiological study of cholera. J Bacteriol 2020; 202:e00086-20 [View Article] [PubMed]
    [Google Scholar]
  25. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  26. Hill AW, Leigh JA. DNA fingerprinting of Streptococcus uberis: a useful tool for epidemiology of bovine mastitis. Epidemiol Infect 1989; 103:165–171 [View Article] [PubMed]
    [Google Scholar]
  27. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
    [Google Scholar]
  28. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article] [PubMed]
    [Google Scholar]
  29. Wilkinson D, Alsharaf L, Thompson S, Paulin A, Takor R et al. Characterization of a Helicobacter pylori strain with high biofilm-forming ability. J Med Microbiol 2023; 72:1710 [View Article] [PubMed]
    [Google Scholar]
  30. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  32. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
    [Google Scholar]
  33. Hossain M, Egan SA, Coffey T, Ward PN, Wilson R et al. Virulence related sequences; insights provided by comparative genomics of Streptococcus uberis of differing virulence. BMC Genomics 2015; 16:334 [View Article] [PubMed]
    [Google Scholar]
  34. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
    [Google Scholar]
  35. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
    [Google Scholar]
  36. Zhou Z, Alikhan N-F, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018; 28:1395–1404 [View Article] [PubMed]
    [Google Scholar]
  37. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 2012; 158:1005–1015 [View Article] [PubMed]
    [Google Scholar]
  38. Keane OM, Budd KE, Flynn J, McCoy F. Pathogen profile of clinical mastitis in Irish milk-recording herds reveals a complex aetiology. Vet Rec 2013; 173:17 [View Article] [PubMed]
    [Google Scholar]
  39. van Tonder AJ, Mistry S, Bray JE, Hill DMC, Cody AJ et al. Defining the estimated core genome of bacterial populations using a Bayesian decision model. PLoS Comput Biol 2014; 10:e1003788 [View Article] [PubMed]
    [Google Scholar]
  40. Lang P, Lefébure T, Wang W, Zadoks RN, Schukken Y et al. Gene content differences across strains of Streptococcus uberis identified using oligonucleotide microarray comparative genomic hybridization. Infect Genet Evol 2009; 9:179–188 [View Article] [PubMed]
    [Google Scholar]
  41. Fenske L, Noll I, Blom J, Ewers C, Semmler T et al. A dominant clonal lineage of Streptococcus uberis in cattle in Germany. Antonie van Leeuwenhoek 2022; 115:857–870 [View Article] [PubMed]
    [Google Scholar]
  42. Ward PN, Holden MTG, Leigh JA, Lennard N, Bignell A et al. Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis. BMC Genomics 2009; 10:54 [View Article] [PubMed]
    [Google Scholar]
  43. Bradley AJ, Green MJ. A study of the incidence and significance of intramammary enterobacterial infections acquired during the dry period. J Dairy Sci 2000; 83:1957–1965 [View Article] [PubMed]
    [Google Scholar]
  44. Smith KL, Todhunter DA, Schoenberger PS. Environmental mastitis: cause, prevalence, prevention. J Dairy Sci 1985; 68:1531–1553 [View Article] [PubMed]
    [Google Scholar]
  45. Tassi R, McNeilly TN, Fitzpatrick JL, Fontaine MC, Reddick D et al. Strain-specific pathogenicity of putative host-adapted and nonadapted strains of Streptococcus uberis in dairy cattle. J Dairy Sci 2013; 96:5129–5145 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001225
Loading
/content/journal/mgen/10.1099/mgen.0.001225
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error