Mammary microbiota of dairy ruminants: fact or fiction?

Abstract

Explorations of how the complex microbial communities that inhabit different body sites might contribute to health and disease have prompted research on the ways the harmonious relationship between a host and its microbiota could be used to keep animals healthy in their production conditions. In particular, there is a growing interest in the bacterial signatures that can be found in the milk of healthy or mastitic dairy cows. The concept of sterility of the healthy mammary gland of dairy ruminants has been challenged by the results of studies using bacterial DNA-based methodology. The newly obtained data have led to the concept of the intramammary microbiota composed of a complex community of diverse bacteria. Accordingly, mammary gland infections are not mere infections by a bacterial pathogen, but the consequence of mammary dysbiosis. This article develops the logical implications of this paradigm shift and shows how this concept is incompatible with current knowledge concerning the innate and adaptive immune system of the mammary gland of dairy ruminants. It also highlights how the concept of mammary microbiota clashes with results of experimental infections induced under controlled conditions or large field experiments that demonstrated the efficacy of the current mastitis control measures.

Figure 1

The mammary gland epithelium is not a mucosal epithelium. A Mucosal surfaces colonized by bacterial communities deploy distinct protective mechanisms. Within the simple columnar epithelium, goblet cells secrete mucus that covers the mucosal surface. The mucus inner and outer layers retain high concentrations of secretory IgA and host antimicrobial peptides (amp) secreted by epithelial cells or specialized cells such as Paneth cells. M cells transport luminal antigens to the dendritic cells beneath. Plasma cells secrete sIgA. T and B cells are present in the lamina propria, some are associated in mucosa-associated lymphoid formations. B The mammary gland epithelium is devoid of mucus, and bovine milk contains low-concentration of IgG. A few macrophages and neutrophils can be found in the lumen, but neutrophils are recruited en masse by inflammation when bacteria proliferate in milk. Bacterial intruders are detected by the epithelium comprised of epithelial cells and intraepithelial dendritic cells. Macrophages and T cells are present in the lamina propria, but organised lymphoid formations are absent from healthy glands.