1887

Abstract

Group B (GBS; ) is a major neonatal and opportunistic bacterial pathogen of humans and an important cause of mastitis in dairy cattle with significant impacts on food security. Following the introduction of mastitis control programmes in the 1950s, GBS was nearly eradicated from the dairy industry in northern Europe, followed by re-emergence in the 21st century. Here, we sought to explain this re-emergence based on short and long read sequencing of historical (1953–1978; =44) and contemporary (1997–2012; =76) bovine GBS isolates. Our data show that a globally distributed bovine-associated lineage of GBS was commonly detected among historical isolates but never among contemporary isolates. By contrast, tetracycline resistance, which is present in all major GBS clones adapted to humans, was commonly and uniquely detected in contemporary bovine isolates. These observations provide evidence for strain replacement and suggest a human origin of newly emerged strains. Three novel GBS plasmids were identified, including two showing >98 % sequence similarity with plasmids from and subsp. , which co-exist with GBS in the human oropharynx. Our findings support introduction of GBS into the dairy population due to human-to-cattle jumps on multiple occasions and demonstrate that reverse zoonotic transmission can erase successes of animal disease control campaigns.

Funding
This study was supported by the:
  • University of Glasgow (Award MVLS DTP PhD Studentship cohort 2017)
    • Principle Award Recipient: ChiaraCrestani
  • Medical Research Council (Award MR/N002660/1)
    • Principle Award Recipient: MarkA Holmes
  • Medical Research Council (Award MR/P007201/1)
    • Principle Award Recipient: MarkA Holmes
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/D/2000217)
    • Principle Award Recipient: SamanthaJ Lycett
  • Biotechnology and Biological Sciences Research Council (Award FORDE/BB/R012075/1)
    • Principle Award Recipient: TayaL Forde
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-09-06
2021-09-16
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References

  1. Seale AC, Bianchi-Jassir F, Russell NJ, Kohli-Lynch M, Tann CJ et al. Estimates of the burden of group B streptococcal disease worldwide for pregnant women, stillbirths, and children. Clin Infect Dis 2017; 65:S200–S219 [View Article]
    [Google Scholar]
  2. Lyhs U, Kulkas L, Katholm J, Persson-Waller K, Saha K et al. Streptococcus agalactiae serotype IV in humans and cattle, Northern Europe. Emerg Infect Dis 2016; 22:2097 [View Article]
    [Google Scholar]
  3. Barkham T, Zadoks RN, Azmai MNA, Baker S, Bich VTN et al. One hypervirulent clone, sequence type 283, accounts for a large proportion of invasive Streptococcus agalactiae isolated from humans and diseased tilapia in Southeast Asia. PLoS Negl Trop Dis 2019; 13:e0007421 [View Article]
    [Google Scholar]
  4. Kwatra G, Cunnington MC, Merrall E, Adrian PV, Ip M et al. Prevalence of maternal colonisation with group B Streptococcus: a systematic review and meta-analysis. Lancet Infect Dis 2016; 16:1076–1084 [View Article]
    [Google Scholar]
  5. van der Mee-Marquet N, Fourny L, Arnault L, Domelier AS, Salloum M et al. Molecular characterization of human-colonizing Streptococcus agalactiae strains isolated from throat, skin, anal margin, and genital body sites. J Clin Microbiol 2008; 46:2906–2911 [View Article]
    [Google Scholar]
  6. Cobo-Ángel CG, Jaramillo-Jaramillo AS, Palacio-Aguilera M, Jurado-Vargas L, Calvo-Villegas EA et al. Potential group B Streptococcus interspecies transmission between cattle and people in Colombian dairy farms. Sci Rep 2019; 9:1–9 [View Article]
    [Google Scholar]
  7. Davies MR, Tran TN, McMillan DJ, Gardiner DL, Currie BJ et al. Inter-species genetic movement may blur the epidemiology of streptococcal diseases in endemic regions. Microbes Infect 2005; 7:1128–1138 [View Article]
    [Google Scholar]
  8. Mweu MM, Nielsen S, Halasa T, Toft N. Annual incidence, prevalence and transmission characteristics of Streptococcus agalactiae in Danish dairy herds. Prev Vet Med 2012; 106:244–250 [View Article]
    [Google Scholar]
  9. Richards VP, Velsko IM, Alam T, Zadoks RN, Manning SD et al. Population gene introgression and high genome plasticity for the zoonotic pathogen Streptococcus agalactiae. Mol Biol Evo 2019; 36:2572–2590 [View Article]
    [Google Scholar]
  10. Riekerink R, Barkema HW, Scholl DT, Poole DE, Kelton DF. Management practices associated with the bulk-milk prevalence of Staphylococcus aureus in Canadian dairy farms. Prev Vet Med 2010; 97:20–28 [View Article]
    [Google Scholar]
  11. Zadoks RN, Fitzpatrick JL. Changing trends in mastitis. Ir Vet J 2009; 62:1–12 [View Article]
    [Google Scholar]
  12. Piepers S, De Meulemeester L, de Kruif A, Opsomer G, Barkema HW et al. Prevalence and distribution of mastitis pathogens in subclinically infected dairy cows in Flanders, Belgium. J Dairy Res 2007; 74:478–483 [View Article]
    [Google Scholar]
  13. Pitkälä A, Haveri M, Pyörälä S, Myllys V, Honkanen-Buzalski T. Bovine mastitis in Finland 2001—prevalence, distribution of bacteria, and antimicrobial resistance. J Dairy Sci 2004; 87:2433–2441 [View Article]
    [Google Scholar]
  14. Sampimon O, Barkema HW, Berends I, Sol J, Lam T. Prevalence of intramammary infection in Dutch dairy herds. J Dairy Res 2009; 76:129–136 [View Article]
    [Google Scholar]
  15. Heymann DL. Control, elimination, eradication and re-emergence of infectious diseases: getting the message right. Bull World Health Organ 2006; 84:82 [View Article]
    [Google Scholar]
  16. Bisharat N, Crook DW, Leigh J, Harding RM, Ward PN et al. Hyperinvasive neonatal group B Streptococcus has arisen from a bovine ancestor. J Clin Microbiol 2004; 42:2161–2167 [View Article]
    [Google Scholar]
  17. Almeida A, Alves-Barroco C, Sauvage E, Bexiga R, Albuquerque P et al. Persistence of a dominant bovine lineage of group B Streptococcus reveals genomic signatures of host adaptation. Environ Microbiol 2016; 18:4216–4229 [View Article]
    [Google Scholar]
  18. Jørgensen HJ, Nordstoga AB, Sviland S, Zadoks RN, Sølverød L et al. Streptococcus agalactiae in the environment of bovine dairy herds–rewriting the textbooks?. Vet Microbiol 2016; 184:64–72 [View Article]
    [Google Scholar]
  19. Weinert LA, Welch JJ, Suchard MA, Lemey P, Rambaut A et al. Molecular dating of human-to-bovid host jumps by Staphylococcus aureus reveals an association with the spread of domestication. Biol Lett 2012; 8:829–832 [View Article]
    [Google Scholar]
  20. Zadoks RN, Middleton JR, McDougall S, Katholm J, Schukken YH. Molecular epidemiology of mastitis pathogens of dairy cattle and comparative relevance to humans. J Mammary Gland Biol Neoplasia 2011; 16:357–372 [View Article]
    [Google Scholar]
  21. Smeds L, Künstner A. ConDeTri-a content dependent read trimmer for Illumina data. PLoS One 2011; 6:e26314 [View Article]
    [Google Scholar]
  22. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  23. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 20131072–1075 [View Article]
    [Google Scholar]
  24. Waskom ML. Seaborn: statistical data visualization. Journal of Open Source Software 2021; 6:3021 [View Article]
    [Google Scholar]
  25. Larsen MV, Cosentino S, Lukjancenko O, Saputra D, Rasmussen S. Benchmarking of methods for genomic taxonomy. J Clin Microbiol 2014; 52:1529–1539 [View Article] [PubMed]
    [Google Scholar]
  26. Richards VP, Lang P, Bitar PDP, Lefébure T, Schukken YH et al. Comparative genomics and the role of lateral gene transfer in the evolution of bovine adapted Streptococcus agalactiae. Infect Genet Evol 2011; 11:1263–1275 [View Article]
    [Google Scholar]
  27. Jain M, Olsen HE, Paten B, Akeson M. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol 2016; 17:239 [View Article]
    [Google Scholar]
  28. Wick RR, Judd LM, Holt KE. Performance of neural network basecalling tools for Oxford Nanopore sequencing. Genome Biol 2019; 20:129 [View Article]
    [Google Scholar]
  29. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comp Biol 2017; 13:e1005595 [View Article]
    [Google Scholar]
  30. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article]
    [Google Scholar]
  31. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article]
    [Google Scholar]
  32. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2006; 23:127–128 [View Article]
    [Google Scholar]
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  34. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article]
    [Google Scholar]
  35. Huson DH. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 1998; 14:68–73 [View Article]
    [Google Scholar]
  36. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article]
    [Google Scholar]
  37. Metcalf BJ, Chochua S, Gertz RE, Hawkins PA, Ricaldi J et al. Short-read whole genome sequencing for determination of antimicrobial resistance mechanisms and capsular serotypes of current invasive Streptococcus agalactiae recovered in the USA. Clin Microbiol Infect 2017; 23:574–e7 [View Article]
    [Google Scholar]
  38. Cunha D, Davies MR, Douarre PE, Rosinski-Chupin I, Margarit I et al. Streptococcus agalactiae clones infecting humans were selected and fixed through the extensive use of tetracycline. Nat Commun 2014; 5:ncomms5544 [View Article]
    [Google Scholar]
  39. Sheppard AE, Vaughan A, Jones N, Turner P, Turner C et al. Capsular typing method for Streptococcus agalactiae using whole-genome sequence data. J Clin Microbiol 2016; 54:1388–1390 [View Article]
    [Google Scholar]
  40. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article]
    [Google Scholar]
  41. Sørensen UBS, Klaas IC, Boes J, Farre M. The distribution of clones of Streptococcus agalactiae (group B streptococci) among herdspersons and dairy cows demonstrates lack of host specificity for some lineages. Vet Microbiol 2019; 235:71–79 [View Article]
    [Google Scholar]
  42. Zeng L, Das S, Burne RA. Utilization of lactose and galactose by Streptococcus mutans: transport, toxicity, and carbon catabolite repression. J Bacteriol 2010; 192:2434–2444 [View Article]
    [Google Scholar]
  43. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: Rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:e000131 [View Article]
    [Google Scholar]
  44. Liu M, Li X, Xie Y, Bi D, Sun J et al. ICEberg 2.0: An updated database of bacterial integrative and conjugative elements. Nucleic Acids Res 2019; 47:D660–D665 [View Article]
    [Google Scholar]
  45. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article]
    [Google Scholar]
  46. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article]
    [Google Scholar]
  47. Li L, Wang R, Huang Y, Huang T, Luo F et al. High incidence of pathogenic Streptococcus agalactiae ST485 strain in pregnant/puerperal women and isolation of hyper-virulent human CC67 strain. Front Microbiol 2018; 9:50 [View Article]
    [Google Scholar]
  48. Luan SL, Granlund M, Sellin M, Lagergård T, Spratt BG et al. Multilocus sequence typing of Swedish invasive group B Streptococcus isolates indicates a neonatally associated genetic lineage and capsule switching. J Clin Microbiol 2005; 43:3727–3733 [View Article]
    [Google Scholar]
  49. Boonyayatra S, Wongsathein D, Tharavichitkul P. Genetic relatedness among Streptococcus agalactiae isolated from cattle, fish, and humans. Foodborne Pathog Dis 2019; 17:137–143 [View Article]
    [Google Scholar]
  50. Hsu JF, Chen CL, Lee CC, Lien R, Chu SM et al. Characterization of group B Streptococcus colonization in full-term and late-preterm neonates in Taiwan. Pediatr Neonatol 2019; 60:311–317 [View Article]
    [Google Scholar]
  51. Wu B, Su J, Li L, Wu W, Wu J et al. Phenotypic and genetic differences among group B Streptococcus recovered from neonates and pregnant women in Shenzhen, China: 8-year study. BMC Microbiol 2019; 19:185 [View Article]
    [Google Scholar]
  52. Yang Y, Liu Y, Ding Y, Yi L, Ma Z et al. Molecular characterization of Streptococcus agalactiae isolated from bovine mastitis in Eastern China. PLoS One 2013; 8:e67755 [View Article]
    [Google Scholar]
  53. European Medicines Agency (EMA) Sales of veterinary antimicrobial agents in 31 European countries in 2017 - Trends from 2010 to 2017. EMA/294674/2019; 2019
  54. Bergmann R, Nerlich A, Chhatwal GS, Nitsche-Schmitz DP. Distribution of small native plasmids in Streptococcus pyogenes in India. Int J Med Microbiol 2014; 304:370–378 [View Article]
    [Google Scholar]
  55. Smith JA, Magnuson RD. Modular organization of the Phd repressor/antitoxin protein. J Bacteriol 2004; 186:2692–2698 [View Article]
    [Google Scholar]
  56. Heng NCK, Ragland NL, Swe PM, Baird HJ, Inglis MA et al. Dysgalacticin: a novel, plasmid-encoded antimicrobial protein (bacteriocin) produced by Streptococcus dysgalactiae subsp. equisimilis. Microbiology 2006; 152:1991–2001 [View Article]
    [Google Scholar]
  57. Swe PM, Heng NCK, Cook GM, Tagg JR, Jack RW. Identification of DysI, the immunity factor of the streptococcal bacteriocin dysgalacticin. Appl Environ Microbiol 2010; 76:7885–7889 [View Article]
    [Google Scholar]
  58. Dogan B, Schukken YH, Santisteban C, Boor KJ. Distribution of serotypes and antimicrobial resistance genes among Streptococcus agalactiae isolates from bovine and human hosts. J Clin Microbiol 2005; 43:5899–5906 [View Article]
    [Google Scholar]
  59. Leal CAG, Queiroz GA, Pereira FL, Tavares GC, Figueiredo HCP. Streptococcus agalactiae sequence type 283 in farmed fish. Brazil Emerg Infect Dis 2019; 25:776 [View Article]
    [Google Scholar]
  60. Delannoy CMJ, Crumlish M, Fontaine MC, Pollock J, Foster G et al. Human Streptococcus agalactiae strains in aquatic mammals and fish. BMC Microbiol 2013; 13:41 [View Article]
    [Google Scholar]
  61. Lowder BV, Guinane CM, Zakour NLB, Weinert LA, Conway-Morris A. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 2009; 106:19545–19550 [View Article] [PubMed]
    [Google Scholar]
  62. Shepheard MA, Fleming VM, Connor TR, Corander J, Feil EJ. Historical zoonoses and other changes in host tropism of Staphylococcus aureus, identified by phylogenetic analysis of a population dataset. PLoS One 2013; 8:e62369 [View Article] [PubMed]
    [Google Scholar]
  63. Katholm J, Bennedsgaard TW, Koskinen MT, Rattenborg E. Quality of bulk tank milk samples from Danish dairy herds based on real-time polymerase chain reaction identification of mastitis pathogens. J Dairy Sci 2012; 95:5702–5708 [View Article] [PubMed]
    [Google Scholar]
  64. Nesbø CL, Dlutek M, Doolittle WF. Recombination in Thermotoga: implications for species concepts and biogeography. Genetics 2006; 172:759–769 [View Article] [PubMed]
    [Google Scholar]
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