The fall and rise of group B Streptococcus in dairy cattle: reintroduction due to human-to-cattle host jumps?

Abstract

ABSTRACTGroup B Streptococcus (GBS; Streptococcus agalactiae) 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 programs 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; n = 44) and contemporary (1997-2012; n = 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% homology with plasmids from Streptococcus pyogenes and Streptococcus dysgalactiae subsp. equisimilis, 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.IMPACT STATEMENTPathogens can jump between humans and animals. Animal domestication and intensification of livestock production systems have caused multiple human to animal spill-over events, sometimes with significant impact on animal health and food production. The most common production-limiting disease of dairy cattle is mastitis, inflammation of the mammary gland, which can be caused by group B Streptococcus, a common commensal and pathogen of humans. Using genomic data from historical and recent isolates, we show that re-emergence of this pathogen in the dairy industry in northern Europe is due to strains with genomic signatures of human host-adaptation, including antimicrobial resistance genes and plasmids. This shows how elimination of animal diseases may be hampered by humans serving as a reservoir of multi-host pathogens, and reverse zoonotic transmission.REPOSITORIESReads for all isolates sequenced in this study have been submitted to the ENA Sequence Read Archive (SRA). SRA accession numbers are included in Table S1, supplementary material, available in the online version of this article.