Associations among milk microbiota, milk fatty acids, milk glycans, and inflammation from lactating Holstein cows

Authors: Coates, Laurynne; DURHAM, SIERRA - University Of California, Davis; Storms, David; Magnuson, Andrew; Van Hekken, Diane; Plumier, Benjamin; Finley, John; Fukagawa, Naomi; Tomasula, Peggy; Lemay, Danielle; Picklo, Matthew; BARILE, DANIELA - University Of California, Davis; Kalscheur, Kenneth; Kable, Mary

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/23/2023
Publication Date: 4/19/2023
Citation: Coates, L.C., Durham, S., Storms, D.H., Magnuson, A.D., Van Hekken, D.L., Plumier, B.M., Finley, J.W., Fukagawa, N.K., Tomasula, M.M., Lemay, D.G., Picklo, M., Barile, D., Kalscheur, K., Kable, M.E. 2023. Associations among milk microbiota, milk fatty acids, milk glycans, and inflammation from lactating Holstein cows. Microbiology Spectrum. 11(3). Article e04020-22. https://doi.org/10.1128/spectrum.04020-22.
DOI: https://doi.org/10.1128/spectrum.04020-22

Interpretive Summary: Bovine milk can harbor microbes that cause mastitis, milk spoilage, and food-borne illness. Fatty acids found in milk can be antimicrobial and milk oligosaccharides can have antiadhesive, prebiotic, and immune-modulatory effects. Relationships among milk microbes, fatty acids, oligosaccharides, and inflammation have been reported in humans. To our knowledge, associations among the milk microbial composition, fatty acids, oligosaccharides, and lactose have not been reported in healthy lactating cows. We found numerous relationships among distinct milk components -- including oligosaccharides, lactose, and fatty acids -- and milk microbes. Some of these milk components also associated with udder inflammation. Future work is needed to determine if inflammation impacts milk composition and if this in turn impacts the milk microbes which might play roles in mammary health. Cow genetics, lactation stage, parity and diet are important factors in the abundance of milk fatty acids and oligosaccharides; therefore determining if these milk components impact milk microbes may provide valuable information for dairy cow management and breeding practices aimed at minimizing harmful and spoilage-causing microbes in raw milk.

Technical Abstract: Milk oligosaccharides (MOs) can be prebiotic and anti-adhesive while fatty acids (MFAs) can be antimicrobial, and both have been associated with milk microbes or mammary inflammation in humans. Relationships between these milk components and milk microbes have not been determined in cows and could help elucidate a novel approach to promote desired milk microbial composition and mammary health. We aimed to determine relationships among milk microbiota, milk components (lactose, MOs and MFAs) and somatic cell counts (SCC) in lactating Holstein cows, using our previously published data. Raw milk samples were collected from cows at three timepoints, ranging from early to late lactation. Data were analyzed using (generalized) linear mixed effects modeling and repeated measures correlation. Microbial diversity was not correlated with MO diversity or MFA diversity. However, many MOs were positively correlated with potentially pathogenic genera (e.g. Corynebacterium, Enterococcus, Pseudomonas), while numerous MOs were negatively correlated with the symbiont Bifidobacterium. The neutral, non-fucosylated MO composed of eight hexoses had a positive relationship with SCC, while lactose had a negative relationship with SCC. No significant relationships between microbial taxa, or microbial '-diversity, and SCC were identified. Lactose had negative relationships with several potentially pathogenic genera: Corynebacterium, Pseudomonas, and Enterococcus. Unsaturated MFA and short chain MFA had mostly negative relationships with potentially pathogenic genera, including Corynebacterium, Pseudomonas, and an unknown Enterobacteriaceae genus, but numerous positive relationships with symbionts Bifidobacterium and Bacteroides. Distinct microbes have unique relationships with distinct milk components, some of which may be impacted by mammary inflammation.