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Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves

BACKGROUND: Calves undergo nutritional, metabolic, and behavioural changes from birth to the entire weaning period. An appropriate selection of weaning age is essential to reduce the negative effects caused by weaning-related dietary transitions. This study monitored the faecal microbiome and plasma...

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Autores principales: Amin, Nida, Schwarzkopf, Sarah, Tröscher-Mußotter, Johanna, Camarinha-Silva, Amélia, Dänicke, Sven, Huber, Korinna, Frahm, Jana, Seifert, Jana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9926800/
https://www.ncbi.nlm.nih.gov/pubmed/36788596
http://dx.doi.org/10.1186/s42523-023-00233-z
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author Amin, Nida
Schwarzkopf, Sarah
Tröscher-Mußotter, Johanna
Camarinha-Silva, Amélia
Dänicke, Sven
Huber, Korinna
Frahm, Jana
Seifert, Jana
author_facet Amin, Nida
Schwarzkopf, Sarah
Tröscher-Mußotter, Johanna
Camarinha-Silva, Amélia
Dänicke, Sven
Huber, Korinna
Frahm, Jana
Seifert, Jana
author_sort Amin, Nida
collection PubMed
description BACKGROUND: Calves undergo nutritional, metabolic, and behavioural changes from birth to the entire weaning period. An appropriate selection of weaning age is essential to reduce the negative effects caused by weaning-related dietary transitions. This study monitored the faecal microbiome and plasma metabolome of 59 female Holstein calves during different developmental stages and weaning times (early vs. late) and identified the potential associations of the measured parameters over an experimental period of 140 days. RESULTS: A progressive development of the microbiome and metabolome was observed with significant differences according to the weaning groups (weaned at 7 or 17 weeks of age). Faecal samples of young calves were dominated by bifidobacterial and lactobacilli species, while their respective plasma samples showed high concentrations of amino acids (AAs) and biogenic amines (BAs). However, as the calves matured, the abundances of potential fiber-degrading bacteria and the plasma concentrations of sphingomyelins (SMs), few BAs and acylcarnitines (ACs) were increased. Early-weaning at 7 weeks significantly restructured the microbiome towards potential fiber-degrading bacteria and decreased plasma concentrations of most of the AAs and SMs, few BAs and ACs compared to the late-weaning event. Strong associations between faecal microbes, plasma metabolites and calf growth parameters were observed during days 42–98, where the abundances of Bacteroides, Parabacteroides, and Blautia were positively correlated with the plasma concentrations of AAs, BAs and SMs as well as the live weight gain or average daily gain in calves. CONCLUSION: The present study reported that weaning at 17 weeks of age was beneficial due to higher growth rate of late-weaned calves during days 42–98 and a quick adaptability of microbiota to weaning-related dietary changes during day 112, suggesting an age-dependent maturation of the gastrointestinal tract. However, the respective plasma samples of late-weaned calves contained several metabolites with differential concentrations to the early-weaned group, suggesting a less abrupt but more-persistent effect of dietary changes on host metabolome compared to the microbiome. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00233-z.
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spelling pubmed-99268002023-02-15 Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves Amin, Nida Schwarzkopf, Sarah Tröscher-Mußotter, Johanna Camarinha-Silva, Amélia Dänicke, Sven Huber, Korinna Frahm, Jana Seifert, Jana Anim Microbiome Research Article BACKGROUND: Calves undergo nutritional, metabolic, and behavioural changes from birth to the entire weaning period. An appropriate selection of weaning age is essential to reduce the negative effects caused by weaning-related dietary transitions. This study monitored the faecal microbiome and plasma metabolome of 59 female Holstein calves during different developmental stages and weaning times (early vs. late) and identified the potential associations of the measured parameters over an experimental period of 140 days. RESULTS: A progressive development of the microbiome and metabolome was observed with significant differences according to the weaning groups (weaned at 7 or 17 weeks of age). Faecal samples of young calves were dominated by bifidobacterial and lactobacilli species, while their respective plasma samples showed high concentrations of amino acids (AAs) and biogenic amines (BAs). However, as the calves matured, the abundances of potential fiber-degrading bacteria and the plasma concentrations of sphingomyelins (SMs), few BAs and acylcarnitines (ACs) were increased. Early-weaning at 7 weeks significantly restructured the microbiome towards potential fiber-degrading bacteria and decreased plasma concentrations of most of the AAs and SMs, few BAs and ACs compared to the late-weaning event. Strong associations between faecal microbes, plasma metabolites and calf growth parameters were observed during days 42–98, where the abundances of Bacteroides, Parabacteroides, and Blautia were positively correlated with the plasma concentrations of AAs, BAs and SMs as well as the live weight gain or average daily gain in calves. CONCLUSION: The present study reported that weaning at 17 weeks of age was beneficial due to higher growth rate of late-weaned calves during days 42–98 and a quick adaptability of microbiota to weaning-related dietary changes during day 112, suggesting an age-dependent maturation of the gastrointestinal tract. However, the respective plasma samples of late-weaned calves contained several metabolites with differential concentrations to the early-weaned group, suggesting a less abrupt but more-persistent effect of dietary changes on host metabolome compared to the microbiome. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00233-z. BioMed Central 2023-02-14 /pmc/articles/PMC9926800/ /pubmed/36788596 http://dx.doi.org/10.1186/s42523-023-00233-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Amin, Nida
Schwarzkopf, Sarah
Tröscher-Mußotter, Johanna
Camarinha-Silva, Amélia
Dänicke, Sven
Huber, Korinna
Frahm, Jana
Seifert, Jana
Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
title Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
title_full Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
title_fullStr Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
title_full_unstemmed Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
title_short Host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
title_sort host metabolome and faecal microbiome shows potential interactions impacted by age and weaning times in calves
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9926800/
https://www.ncbi.nlm.nih.gov/pubmed/36788596
http://dx.doi.org/10.1186/s42523-023-00233-z
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