Composition and co-occurrence patterns of the microbiota of different niches of the bovine mammary gland: potential associations with mastitis susceptibility, udder inflammation, and teat-end hyperkeratosis

Abstract

Background: Within complex microbial ecosystems, microbe-microbe interrelationships play crucial roles in determining functional properties such as metabolic potential, stability and colonization resistance. In dairy cows, microbes inhabiting different ecological niches of the udder may have the potential to interact with mastitis pathogens and therefore modulate susceptibility to intramammary infection. In the present study, we investigated the co-occurrence patterns of bacterial communities within and between different niches of the bovine mammary gland (teat canal vs. milk) in order to identify key bacterial taxa and evaluate their associations with udder health parameters and mastitis susceptibility. Results: Overall, teat canal microbiota was more diverse, phylogenetically less dispersed, and compositionally distinct from milk microbiota. This, coupled with identification of a large number of bacterial taxa that were exclusive to the teat canal microbiota suggested that the intramammary ecosystem, represented by the milk microbiota, acts as a selective medium that disfavors the growth of certain environmental bacterial lineages. We further observed that the diversity of milk microbiota was negatively correlated with udder inflammation. By performing correlation network analysis, we identified two groups of phylogenetically distinct hub species that were either positively (unclassified Bacteroidaceae and Phascolarctobacterium) or negatively (Sphingobacterium) correlated with biodiversity metrics of the mammary gland (MG). The latter group of bacteria also showed positive associations with the future incidence of clinical mastitis. Conclusions: Our results provide novel insights into the composition and structure of bacterial communities inhabiting different niches of the bovine MG. In particular, we identified hub species and candidate foundation taxa that were associated with the inflammatory status of the MG and/or future incidences of clinical mastitis. Further in vitro and in vivo interrogations of MG microbiota can shed light on different mechanisms by which commensal microbiota interact with mastitis pathogens and modulate udder homeostasis.