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Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows

Milk oligosaccharides (MOs) can be prebiotic and antiadhesive, while fatty acids (MFAs) can be antimicrobial. Both have been associated with milk microbes or mammary gland inflammation in humans. Relationships between these milk components and milk microbes or inflammation have not been determined f...

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Autores principales: Coates, Laurynne C., Durham, Sierra D., Storms, David H., Magnuson, Andrew D., Van Hekken, Diane L., Plumier, Benjamin M., Finley, John W., Fukagawa, Naomi K., Tomasula, Peggy M., Lemay, Danielle G., Picklo, Matthew J., Barile, Daniela, Kalscheur, Kenneth F., Kable, Mary E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269560/
https://www.ncbi.nlm.nih.gov/pubmed/37074179
http://dx.doi.org/10.1128/spectrum.04020-22
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author Coates, Laurynne C.
Durham, Sierra D.
Storms, David H.
Magnuson, Andrew D.
Van Hekken, Diane L.
Plumier, Benjamin M.
Finley, John W.
Fukagawa, Naomi K.
Tomasula, Peggy M.
Lemay, Danielle G.
Picklo, Matthew J.
Barile, Daniela
Kalscheur, Kenneth F.
Kable, Mary E.
author_facet Coates, Laurynne C.
Durham, Sierra D.
Storms, David H.
Magnuson, Andrew D.
Van Hekken, Diane L.
Plumier, Benjamin M.
Finley, John W.
Fukagawa, Naomi K.
Tomasula, Peggy M.
Lemay, Danielle G.
Picklo, Matthew J.
Barile, Daniela
Kalscheur, Kenneth F.
Kable, Mary E.
author_sort Coates, Laurynne C.
collection PubMed
description Milk oligosaccharides (MOs) can be prebiotic and antiadhesive, while fatty acids (MFAs) can be antimicrobial. Both have been associated with milk microbes or mammary gland inflammation in humans. Relationships between these milk components and milk microbes or inflammation have not been determined for cows and could help elucidate a novel approach for the dairy industry to promote desired milk microbial composition for improvement of milk quality and reduction of milk waste. We aimed to determine relationships among milk microbiota, MFAs, MOs, lactose, and somatic cell counts (SCC) from Holstein cows, using our previously published data. Raw milk samples were collected at three time points, ranging from early to late lactation. Data were analyzed using linear mixed-effects modeling and repeated-measures correlation. 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. Conversely, many MOs were positively correlated with potentially pathogenic genera (e.g., Corynebacterium, Enterococcus, and Pseudomonas), and numerous MOs were negatively correlated with the symbiont Bifidobacterium. The neutral, nonfucosylated MO composed of eight hexoses had a positive relationship with SCC, while lactose had a negative relationship with SCC. One interpretation of these trends might be that in milk, MFAs disrupt primarily pathogenic bacterial cells, causing a relative increase in abundance of beneficial microbial taxa, while MOs respond to and act on pathogenic taxa primarily through antiadhesive methods. Further research is needed to confirm the potential mechanisms driving these correlations. IMPORTANCE Bovine milk can harbor microbes that cause mastitis, milk spoilage, and foodborne 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 for humans. To our knowledge, associations among the milk microbial composition, fatty acids, oligosaccharides, and lactose have not been reported for healthy lactating cows. Identifying these potential relationships in bovine milk will inform future efforts to characterize direct and indirect interactions of the milk components with the milk microbiota. Since many milk components are associated with herd management practices, 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.
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spelling pubmed-102695602023-06-16 Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows Coates, Laurynne C. Durham, Sierra D. Storms, David H. Magnuson, Andrew D. Van Hekken, Diane L. Plumier, Benjamin M. Finley, John W. Fukagawa, Naomi K. Tomasula, Peggy M. Lemay, Danielle G. Picklo, Matthew J. Barile, Daniela Kalscheur, Kenneth F. Kable, Mary E. Microbiol Spectr Research Article Milk oligosaccharides (MOs) can be prebiotic and antiadhesive, while fatty acids (MFAs) can be antimicrobial. Both have been associated with milk microbes or mammary gland inflammation in humans. Relationships between these milk components and milk microbes or inflammation have not been determined for cows and could help elucidate a novel approach for the dairy industry to promote desired milk microbial composition for improvement of milk quality and reduction of milk waste. We aimed to determine relationships among milk microbiota, MFAs, MOs, lactose, and somatic cell counts (SCC) from Holstein cows, using our previously published data. Raw milk samples were collected at three time points, ranging from early to late lactation. Data were analyzed using linear mixed-effects modeling and repeated-measures correlation. 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. Conversely, many MOs were positively correlated with potentially pathogenic genera (e.g., Corynebacterium, Enterococcus, and Pseudomonas), and numerous MOs were negatively correlated with the symbiont Bifidobacterium. The neutral, nonfucosylated MO composed of eight hexoses had a positive relationship with SCC, while lactose had a negative relationship with SCC. One interpretation of these trends might be that in milk, MFAs disrupt primarily pathogenic bacterial cells, causing a relative increase in abundance of beneficial microbial taxa, while MOs respond to and act on pathogenic taxa primarily through antiadhesive methods. Further research is needed to confirm the potential mechanisms driving these correlations. IMPORTANCE Bovine milk can harbor microbes that cause mastitis, milk spoilage, and foodborne 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 for humans. To our knowledge, associations among the milk microbial composition, fatty acids, oligosaccharides, and lactose have not been reported for healthy lactating cows. Identifying these potential relationships in bovine milk will inform future efforts to characterize direct and indirect interactions of the milk components with the milk microbiota. Since many milk components are associated with herd management practices, 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. American Society for Microbiology 2023-04-19 /pmc/articles/PMC10269560/ /pubmed/37074179 http://dx.doi.org/10.1128/spectrum.04020-22 Text en https://doi.org/10.1128/AuthorWarrantyLicense.v1This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.
spellingShingle Research Article
Coates, Laurynne C.
Durham, Sierra D.
Storms, David H.
Magnuson, Andrew D.
Van Hekken, Diane L.
Plumier, Benjamin M.
Finley, John W.
Fukagawa, Naomi K.
Tomasula, Peggy M.
Lemay, Danielle G.
Picklo, Matthew J.
Barile, Daniela
Kalscheur, Kenneth F.
Kable, Mary E.
Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows
title Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows
title_full Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows
title_fullStr Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows
title_full_unstemmed Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows
title_short Associations among Milk Microbiota, Milk Fatty Acids, Milk Glycans, and Inflammation from Lactating Holstein Cows
title_sort associations among milk microbiota, milk fatty acids, milk glycans, and inflammation from lactating holstein cows
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269560/
https://www.ncbi.nlm.nih.gov/pubmed/37074179
http://dx.doi.org/10.1128/spectrum.04020-22
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